Adaptation

Lloyd
Natural selection causes adaptation, the fit between an

organism and its environment. For example, the white and
grey coloration of snowy owls living and breeding around the
Arctic circle provides camouflage from both predators and
prey. In this Element, we explore a variety of such outcomes
of the evolutionary process, including both adaptations and The Philosophy of
alternatives to adaptations, such as nonadaptive traits inherited
from ancestors. We also explore how the concept of adaptation Biology
is used in evolutionary psychology and in animal behavior,
and the adequacy of methods used to confirm evolutionary
accounts of human traits and behaviors.
Adaptation
Adaptation
About the Series Series Editors
This Cambridge Elements series provides Grant Ramsey
concise and structured introductions to KU Leuven, Belgium
Elisabeth A. Lloyd
all of the central topics in the philosophy Michael Ruse
of biology. Contributors to the series Florida State
are cutting-edge researchers who offer University
balanced, comprehensive coverage
of multiple perspectives, while also
developing new ideas and arguments
from a unique viewpoint.
Cover image: Ascidiae from Kunstformen der Natur (1904)

by Ernst Haeckel, public domain Downloaded from https://www.cambridge.org/core. IP address: 201.102.134.53, on 30 Apr 2021 at 23:22:53, subject toISSN 2515-1126 (online)
the Cambridge Core
terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/9781108634953 ISSN 2515-1118 (print)
Downloaded from https://www.cambridge.org/core. IP address: 201.102.134.53, on 30 Apr 2021 at 23:22:53, subject to the Cambridge Core
terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/9781108634953
Elements in the Philosophy of Biology
edited by
Grant Ramsey
KU Leuven
Michael Ruse
Florida State University
ADAPTATION
Elisabeth A. Lloyd
Indiana University
University Printing House, Cambridge CB2 8BS, United Kingdom
One Liberty Plaza, 20th Floor, New York, NY 10006, USA
477 Williamstown Road, Port Melbourne, VIC 3207, Australia
314–321, 3rd Floor, Plot 3, Splendor Forum, Jasola District Centre,
New Delhi – 110025, India
79 Anson Road, #06–04/06, Singapore 079906
Cambridge University Press is part of the University of Cambridge.

It furthers the University’s mission by disseminating knowledge in the pursuit of
education, learning, and research at the highest international levels of excellence.
www.cambridge.org
Information on this title: www.cambridge.org/9781108727549
DOI: 10.1017/9781108634953
© Elisabeth A. Lloyd 2021
This publication is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without the written
permission of Cambridge University Press.
First published 2021
A catalogue record for this publication is available from the British Library.
ISBN 978-1-108-72754-9 Paperback
ISSN 2515-1126 (online)
ISSN 2515-1118 (print)
Cambridge University Press has no responsibility for the persistence or accuracy of
URLs for external or third-party internet websites referred to in this publication
and does not guarantee that any content on such websites is, or will remain,
accurate or appropriate.
Adaptation
DOI: 10.1017/ 9781108634953

First published online: June 2021
Elisabeth A. Lloyd
Indiana University
Abstract: Natural selection causes adaptation, the fit between an

organism and its environment. For example, the white and grey
coloration of snowy owls living and breeding around the Arctic Circle
provides camouflage from both predators and prey. In this Element, we
explore a variety of such outcomes of the evolutionary process,
including both adaptations and alternatives to adaptations, such as
nonadaptive traits inherited from ancestors. We also explore how the
concept of adaptation is used in evolutionary psychology and in animal
behavior, and the adequacy of methods used to confirm evolutionary
accounts of human traits and behaviors.
Keywords: evolutionary adaptation, evolutionary causes, development and

evolution, evolutionary by-products, methodological adaptationism
© Elisabeth A. Lloyd 2021

ISBNs: 9781108727549 (PB), 9781108634953 (OC)
ISSNs: 2515-1126 (online), 2515-1118 (print)
Contents
1 What Are Adaptations? 1
2 Evolutionary Factors 15
3 Adaptationism and the Logic of Research Questions 34
4 Case Studies Showing the Inadequacy of Methodological

Adaptationism 44
References 82
Adaptation 1
1 What Are Adaptations?

1.1 Adaptation at the Organismic Level
Picture a woodpecker hanging on a tree. What do you see them doing?
They pound their beaks into the bark of the tree at a rate of up to twenty
times per second, so hard that the sound carries clearly throughout the
neighborhood.
Woodpeckers have a number of special adaptations to aid them in getting
the food they eat, which is grubs, insects, and worms that live underneath the
bark of trees. What special adaptations help the woodpecker get at these
insect foods they like to eat? And how do they escape the expected harm of
slamming their heads and beaks up against a hard tree at a rapid rate for tens
of minutes at a time? Wouldn’t this scramble their brains, damage their eyes,
and cause brain injury? Moreover, how do they reach inside the holes once
they are made? Their closest relatives, the honeyguides, do not have
extended tongues, but they do eat grubs and even beeswax from beehives.
Let us consider these adaptive challenges met by the woodpecker.
First, the woodpecker has evolved a chisel-like tip on its beak to help
drill holes in the trees in which its food lives. But wouldn’t this repeated
trauma to the head of the woodpecker damage the brain during this harsh
drilling routine? No, because the woodpecker has also evolved a spongy
lining to its skull, which has, in addition, thickened to absorb the drilling
vibrations.
Moreover, the eyes of the woodpecker have also evolved special mem-
branes to protect them during the harsh, repeated drilling motion. Finally,
the woodpecker’s tongue has evolved a barb at the end, and sticky saliva so
that it can gather the insects inside the wood and bark of the trees after it
drills its holes.
And there are additional special adaptations possessed by woodpeckers
(also used by hummingbirds for identical purposes): The hyoid apparatus is
lengthened. The hyoid apparatus is made up of a series of bones, muscles,
and cartilage, connected to the tongue, that allow the tongue to extend to
great lengths in nearly all of the woodpecker species. The hyoid apparatus
wraps around the base of the skull and over and around the top of the skull,
making the “base” of the tongue wrap fully around the skull of the wood-
pecker. In the red-bellied woodpecker, the tongue extends three times the
length of its bill. We can see that the woodpecker species are specially
adapted for their ecological niche of eating grubs and insects from trees
with a suite of specially adapted traits enabling them to exploit this otherwise
inaccessible source of food.
2 Elements in the Philosophy of Biology
1.2 Evolutionary Models

Our scientific challenge is to explain how the woodpecker evolved all these
special adaptations for its life of eating bugs from under the bark of trees. Any
study of adaptation in evolution must rely on a very clear understanding of the
process of natural selection, and also what kinds of evidence are desirable for
demonstrating that a trait is an adaptation. We will review the basics of these
selective explanations in this section, as well as the kinds of evidence that
support such explanations.
What happens during a simple process of natural selection, according to
evolutionary biologists? In all cases, we start with a population of entities,
whether they are plants or animals, bacteria within our guts or groups of flour
beetles, and variation in traits within that population.
Detailed aspects of the environment then constrain the reproductive success
of some of those entities (call them the losing ones), while allowing or encour-
aging the reproduction of others among the population (call them the winning
ones), depending upon their key features that vary. Under conditions where the
key features of the winning and losing entities are reliably passed on to the next
generation during reproduction, evolution by natural selection will occur within
the population. Specifically, the proportion of entities with certain key winning
features will grow, while the proportion of entities with the losing key features
will shrink, over time (Futuyma & Kirkpatrick 2017; Griffiths et al. 2005). This
embodies a simple process of natural selection, though not its only manifestation.
It turns out that selection does not act on traits separately, but rather as
clusters or combinations. For example, in the woodpecker, it does no good to
have an extra-long tongue if you do not also have the spongy protective skull to
protect your brain from repetitive drilling.
One terminological point that we need to get to right away is: What exactly do
we mean when we call something an “adaptation”? Do we mean that any trait that
comes out of a selection process is an adaptation? Or do we mean that only traits
that are “engineered” or whose form is changed by selection are adaptations?
Consider some examples to make the meaning of “adaptation” clearer.
Many have learned about the case of “industrial melanism” involving the
peppered moths in England. The population of moths was exposed to tree
trunks blackened by the soot from factories, and the population of peppered
moths went from mostly white moths to mostly black moths. This was due to
natural selection on variation in traits in the form of birds eating the visible
white moths that were resting on the black trees. Thus, the newly black
dominance in the population can be considered an adaptation as a result of
the selection process. But note that there are no new mechanisms and no new
Adaptation 3
forms of moth in this case: There is no engineering or cumulative adaptation

arising from the bird predation. Giorgio Airoldi calls this a case of “pure
selection” (2018). All we have is a change in population distribution of the
black and white moths. It is surely correct to call this a process of natural
selection, and under the “selection-product” meaning of “adaptation,” also
correct to say that the black-dominance in the population is an adaptation. This
“product of selection” (or “selection-product”) definition views any outcome
of a process that affects fitness in a positive manner as an adaptation. But it
seems incorrect to say that there is a cumulative or engineering adaptation
arising from this selection process.
Note the contrast with the woodpecker case. In the woodpeckers, we got
a whole list of engineering adaptations that resulted, we believe, from natural
selection processes and unknown amounts of developmental factors producing
additional variation for selection to act on in these ancestral species of insect-
ivores (species that eat insects). This “engineering” definition of adaptation has
been dominant in the literature for many years and is the definition used in
George C. Williams’ ground-breaking book, Adaptation and Natural Selection
(1966). Notably, Richard Lewontin (1978) and Stephen Jay Gould,1 well-
known critics of adaptationist research, also used the “engineering” definition
of adaptation. The key relevant feature of an engineering adaptation is that it
involves a mechanism or complex feature of some kind, built up cumulatively
from simpler features, whereas the product of selection or distributive definition
of adaptation involves simply a change or shift in allele frequency, one that
could be unrelated to building a revised mechanism (Williams 1966, Lewontin
1978, Gould and Vrba 1982).
The “engineering” account requires that the adaptive account explain the
adaptive feature(s) or modification(s) acquired through the selective process
over time, its “engineering” history of its complex and built-up adaptive traits.
Thus, the idea of an evolutionary function is tied intimately to the definition of
adaptation itself. This is in accordance, for example, with John Maynard Smith’s
idea that “the ‘function’ of an organ is taken to mean those of its effects which have
been responsible for its evolution by natural selection” (1978, p. 23). This could
apply either to selection-product or engineering views of adaptation. But contrary
to the usage of some other philosophers, I will be using exclusively the engineering
definitions of adaptation and function throughout this Element, unless otherwise
noted. See Table 1.1 for a more complete set of definitions below.
Later in this section we will talk about the notion of “function,” but first let us
consider some examples.
1
Gould and Lewontin 1979.
Table 1.1 Definitions2
Term Definition
Aptation a trait that increases fitness (aptation for x – by x-ing).
(If a trait is an aptation but not an adaptation, then
it was not selected in the past for x-ing, and is an
exaptation for x-ing).
Non-Aptation a trait that does not increase fitness (but may do so in
future)
“Engineering” a trait that involves a mechanism or complex feature
Adaptation of some kind, built up cumulatively from simpler
features through natural selection processes. These
types of adaptation involve both the etiological
and the systems analysis types of ‘function’
(Williams 1966, Lewontin 1978, Gould and Vrba
1982; Lloyd 1988)
“Product of Selection” a trait that involves simply a change or shift in allele
Adaptation frequency, one that could be unrelated to building
a revised mechanism (Williams 1966, Lewontin
1978, Gould and Vrba 1982)
Exaptation a trait with no direct engineering function for x,
which nevertheless increases fitness by x-ing
(Gould and Vrba 1982)
Function a trait has the engineering (evolutionary) function of
x-ing, if x-ing increased fitness in evolutionary
history, and the increased fitness explains the
prevalence of the x-ing complex or engineering
trait
Secondary Adaptation a trait modified by natural selection (for x-ing, say)
because of its contribution to fitness (by x-ing),
where the trait so-modified existed, before
modification, for a different reason than the role it
came to have in x-ing
Spandrel a trait is a “spandrel” if the trait in question (the
trait that was pressed into service) for x-ing
(where x-ing increases fitness but was not
selected for its fitness contributions and hence
does not have the function of x-ing) has no direct
engineering function at all (a subset of
exaptation).
2
Thanks to an anonymous reviewer for help with these definitions.
Adaptation 5
Let’s imagine, as Darwin did, a pack of wolves, some of which were swifter
and slimmer than others in the pack: “[T]he swiftest and slimmest wolves would
have the best chance of surviving, and so be preserved or selected” (Darwin p. 90,
1859).3 They would do better in the evolutionary long run, reproducing more
often and having healthier pups, thereby contributing more genes for the structure
of their legs for swifter running to future generations through the process of
natural selection. That’s how the wolves became such swift runners over evolu-
tionary time, able to take down very swift prey. In other words, we are claiming
that “swiftness” is an evolutionary engineering set of adaptations in wolves,
evolved by natural selection over evolutionary time. We have a type of biological
model, in the claim of the process of evolution by natural selection, one that we
can sketch and consider for its evidential weight. Or, we can ask, more specific-
ally, what kinds of evidence would we need to establish a trait like swiftness as an
evolutionary adaptation in wolves?
Now that we’ve had a chance to consider some adaptations in nature, we can
see the various types of evidence needed to establish a trait as an adaptation. As
Darwin argued, and as was later elaborated after the discovery of genetics, the key
ingredients of the most basic natural selection model type in evolution are
represented in Box 1.1.
We start with a population of organisms (and we fill in that blank in the
selection model outline by specifying which population we are considering),
and we have descriptions of traits to focus on, as well as claims of how these
traits are heritable or based in genetics (filling in the appropriate blanks of the
selection model outline). We also need claims about how these traits are related
to fitness, usually supplied in the form of a mechanism explaining how the trait
BOX 1.1 NATURAL SELECTION MODEL OUTLINE
population [____]
variation in trait(s) [____]
genetic/cellular basis [____]
connection or mechanism between trait(s) and fitness [____]
selection pressure or environment [____]
3
“[T]ake the case of a wolf, which preys on various animals, securing some by craft, some by strength,
and some by fleetness; and let us suppose that the fleetest prey, a deer for instance, had from any
change in the country, increased in numbers, or that other prey had decreased in numbers, during that
season of the year when the wolf is hardest pressed for food. I can under such circumstances see no
reason to doubt that the swiftest and slimmest wolves would have the best chance of surviving, and so
be preserved or selected . . . . I can see no more reason to doubt this, than that man can improve the
fleetness of his greyhounds by careful and methodical selection” (pp. 90–91, 1859).
increases fitness, as well as a description of a selection scenario that describes

how pressure from an environment imposes on a population in a way that leads
to changes in trait frequencies over time, as we saw with the fleet wolves and the
woodpeckers.
As we can see, a variety of types of evidence might be required to substantiate
the claims filling in the blanks of the selection model. Each of these claims, such
as how the trait is related to fitness, and what the selection scenario is, needs to
be substantiated with empirical or observational evidence.
Evolutionists Barry Sinervo and Alexandra Basolo (1996) offer a helpful
discussion of what they think of as important evidence for adaptations. They
start with a consideration of whether a particular trait of an organism is “opti-
mal.” Whether a trait is “optimal” is a calculation that depends on a separate
model of optimality. Each optimal trait is the best-engineered trait it could be,
given the constraints of the system, including developmental constraints and
genetic constraints, and the job it needs to do, or the function it needs to fulfil.
Perhaps we can understand optimality better by looking at one of its most
famous examples: dung fly mating times. Because males of this species of
yellow dung fly mate with more than one female, they like to spend as little
time as possible with each female, maximizing their chances at multiple mat-
ings with other females on other cow pies. However, the males also need to
copulate with the females long enough to displace previous males’ sperm inside
the female’s reproductive tract. The ability to do this depends on the size of the
male. It is in the first male’s interest to stick around after mating and guard her
against mating soon with another male. Geoff Parker and colleagues (Charnov
and Parker 1995) predicted that how long the male would copulate would
depend on how far away the other cow pies were – in other words, how far
away the other females were – and on how large the male was. This is an
optimality model, in fact, a physical/biological version of an economics model
called “marginal value theorem,” and they were assuming that the male would
optimize its behavior in terms of mating efficiency. And lo and behold, when
they experimentally manipulated the dung fly males and the mating opportun-
ities, they found that the males copulated with the females for the predicted
periods of time (Charnov and Parker 1995).
Optimality models obviously make a number of assumptions about the
systems they model, not least that the traits they model are engineering adapta-
tions, but these models can be fruitful for research.
If we do assume that these traits are engineering adaptations, we may still
want to know what the state of the traits was before the evolution of the
adaptation in question. What did the species look like before the trait evolved
the way it did?
Adaptation 7
Understanding this involves reconstructing the ancestors of the current popu-

lation and trying to see what traits they had, without their relying on the
adaptation we are studying. This may involve looking back into the ancestral
tree of the population and seeing who is closely and more distantly related to the
population, to see who had related traits and who did not. By doing this
comparative work in phylogenetics (the study of the relatedness and traits of
entities like species and lineages), we can better see what may be new in this
species, lineage, or population of entities.
When studying the evolution of an adaptation, it may be ideal to do some
experiments, as Sinervo and Basolo do (1996). The best experiments on adap-
tations often do two things at the same time:
(1) They manipulate key features of the environment, the very features that the
trait is believed to be an adaptation for dealing with.
(2) And they manipulate the phenotype or appearance of the traits of the
species being studied. So, for example, if we are studying the adaptation
of the size of organisms, we would want to do an experiment that involves
populations of both small- and large-size organisms.
When these experiments are done, it may be possible to determine which

phenotype it is best to have in which environment. In other words, an
organism may have higher fitness or reproductive success when it is large
and living in large ponds, while a smaller organism may have higher fitness
or reproductive success when it is living in smaller ponds. Thus, by
manipulating both the environment and the phenotype, we are able to
determine how the fitness parameter varies with the trait in a given envir-
onment. This is just the information we need in order to fill in the selection
model.
Knowing all this, we might be able to discern whether the trait is an adapta-
tion, that is, whether it evolved to serve a particular function in that species,
given a certain environment. John Maynard Smith’s idea is that “the ‘function’
of an organ is taken to mean those of its effects which have been responsible for
its evolution by natural selection” (1978, p. 23).
In his review of the concept, Colin Allen offers us two main philosophical
accounts of function:
Etiological approaches to function look to a causal-historical process of

selection; functions are identified with those past effects that explain the
current presence of a thing by means of a historical selection process (typic-
ally natural selection in the case of biological function).
Systems-analysis approaches invoke an ahistorical, engineering style of
analysis of a complex system into its components. Functions of components
are identified with their causal contributions to broader capacities of the

system. (emphasis added; Allen 2002, p. 375)4
Note that both the engineering adaptations and product of selection or effects
type of adaptation, introduced above and present in Table 1.1, fall under
etiological approaches to function; they both invoke the historical selection
process to explain the current presence of a trait. The engineering adaptations
also appeal to design analyses often identified with the systems-analysis
notion of function. Thus, engineering adaptations in evolution appeal to
both etiological and systems-analysis approaches to function in the philo-
sophical senses just presented (Lloyd 1988; Williams 1966; Lewontin 1978;
Gould 2002). Knowing all this, in addition, we may also be able to determine
whether the trait is being maintained in current populations through current
selection.
Adaptation is an “onerous concept,” according to George C. Williams in
his 1966 foundational text on the notion. He thought that a burden of proof
rested on those claiming an adaptation and that adaptation should not be
assumed to exist at the outset of biological investigation, just because
a benefit could be perceived. We can look at how this burden of proof plays
out by considering evidence supporting claims of engineering adaptations in
guppies.
1.2 Confirming Evolutionary Models

1.2.1 Model Fit
There are several basic types of supporting evidence and confirmation:

The first type of evidence that can support the type of natural selection model
we have just described is “model fit,” that is, where the predictions of, for
example, an optimality model “fit” or predict the outcome that we find in the
real population of organisms. We can have model fit of selective models as well,
where, after filling in all the blanks in our natural selection model outline in Box
1.1, we can predict correctly what the model outcome would be. We need an
example to help understand this.
Biologists David Reznick, John Endler, and colleagues studied life history
traits in guppies (see Figure 1.1). “Life history” traits are simply those traits
involving the main stages in life, such as development to maturity, reproduction,
and aging (Reznick and Travis 1996; Endler 1978).
4
This latter systems definition is most often identified as a “Cummins function” approach
(Cummins 1975). See Larry Wright (1973) for more on the etiological approach.
Adaptation 9
Figure 1.1 Guppies like those studied by Sinervo and Basolo (1996)
They studied the hypothesis that life history traits in the guppies were actually
adaptations to stage-specific predation that were caused by predators, in other
words, adaptations to the rate at which the predators of guppies killed the
guppies. Reznick and his colleagues studied two communities that differed in
their predators. One type had cichlids as predators – fish that prey heavily on
adult-stage guppies – while the other had Rivulus fish that preyed only lightly
on guppies, and when they did, it was mostly on juvenile guppies.
Evolutionary theories concerning predation and trade-offs between early and
later reproduction made it possible to make predictions about life histories.
The evolutionists investigated the correlation between guppy life histories
and the type of predator communities. The first prediction was that an increase
in predation on the adults, like that found with the cichlids, would select for
a decrease in the age at sexual maturity.
As we can see from Figure 1.2, the measurements from the guppies caught in
the wild revealed differences in guppy life histories that were consistent with the
predictions. In other words, there was good “model fit.” Guppies from Rivulus
localities, where predation was low, were older at maturity than their counter-
parts from Cichlid localities, where predation was high, which gave the guppies
less chance to mature and breed at older ages. Thus, natural selection, according
to the hypothesis, evolved guppies that matured earlier and were able to breed at
younger ages in the high-predation environment, just as the model predicted.
This is an example of directional selection, as illustrated in Figure 1.3. Simple
directional or stabilizing selection usually produces peaks in the distribution
curves of a trait, and with directional selection, the population average moves
Cren/Riv (Days) Eleo/R-M (Days) Cren/Riv (mg) Eleo/R-M (mg)

90 95 300
A B
150
85
90 140
250
80
130
85
75 120
200
Female Age 80 Female Size
70 (days) (mg) 110
65 75 150 100
70 65
C D
100 65 60
60
55
90 55
Male Size at 50 Male Age at
Maturity 50 Maturity
80 45 45
Riv Cren Riv Cren
Riv/Macro Eleo Riv/Cren Riv/Macro Eleo
R-M/Eleo
Figure 1.2 Decrease of age at sexual maturity depending on predator (Reznick

and Travis 1996, p. 266): Least square means (+1 standard error) for the age and
size at maturity and size at first birth in females from high- versus low-predation
environments. See caption in Reznick and Travis for more information. Think of
the predation rates as going from low to high from left to right on the x-axis. The
stippled lines represent the means for the Low (Riv/Macro) versus high (Eleo)
predation sites. The solid lines are the corresponding values for the high (Cren) and
low (Riv) predation sites. All differences between the high- and low-predation
sites were significant. (A) Female age at first birth (days). (B) Female size at first
birth (wet weight in mg). (C) Male size at maturity (wet weight in mg). (D) Male
age at maturity (days).
over to a new, more desirable, value. (We will examine a case of stabilizing
selection in Section 4). Note that this account assumes that the traits are
genetically controlled rather than arising from phenotypic plasticity.
This guppy reproduction case is a good example of the good fit of
a selective evolutionary model prediction with the data from animals taken
from the wild.
Adaptation 11
Figure 1.3 Selection regimes: stabilizing vs. directional selection5
1.2.2 Independent Support for Aspects of the Model
As exciting as it is to have selective model predictions be supported by evidence

from the wild, there is another distinct type of evidence that can support
selection models that may, in many cases, be even more important.
I call it ‘independent support for aspects of the model.’
For example, any selection model includes the assumption that the trait under
selection is “heritable,” or reliably passed from generation to generation. This
5
Image was taken from here: https://courses.lumenlearning.com/boundless-biology/chapter/adap
tive-evolution/ License: CC BY-SA: Attribution-ShareAlike Link to License: https://creativecom
mons.org/licenses/by-sa/4.0/legalcode
usually means that the trait under selection has a “genetic basis,” or, more
accurately, some representation in the cells, development, or genes of the
entities under selection.
In the guppy case, Reznick and his colleagues evaluated the genetic basis of
the differences in life history traits by doing a simple experiment: They
examined the second generation of the wild guppies, which they had bred
and grown up in the laboratory. They found that the traits in question did
reappear in this later generation, despite the fact that the guppies were
removed from their standard selective environment and grew up in a simple
glass tank. Thus, the assumption of heritability, or a genetic basis (a genetic/
developmental/cellular basis) for the trait, was independently supported.
What this claim of “independent support” means is that regardless of how
the predictions of the selection model turned out in the wild, the claim that the
trait had a heritable basis was supported with lab evidence independent of that
prediction.
We could take several of the features in our natural selection model and check
to see whether they had independent observational, theoretical, or experimental
evidence to support them. These would all count as “independent evidence for
aspects of the model.”
1.2.3 Variety of Evidence
A third distinct type of evidence for selection models is variety of evidence, of

which there are two kinds. The Variety of Fit amounts to the claim that
predictions or outcomes under different conditions using the model are verified.
We can see how this works in the guppy case.
Reznick and colleagues (Reznick and Travis 1996; Endler 1978) predicted
that the guppies from the high-predation sites would devote a higher percentage
of consumed resources to reproduction. The model predictions were confirmed
in the first experiment, but then, in addition, the model predictions were
confirmed in forty new locations, thus adding many cases amounting to
a variety of fit (Reznick and Travis 1996).
Variety of Fit
Model predictions confirmed in a variety of locations can bolster support for
a hypothesis. In a further example, when Reznick and colleagues tested guppy
life history evolutionary traits across six independently evolved lineages in six
independent stream locations in Trinidad, they bolstered their conclusions about
those life history traits (El-Sabaawi et al. 2012).
Adaptation 13
BOX 1.2 FILLED-IN NATURAL SELECTION MODEL
Population [guppy population]

Trait [age of maturity]
Heritability/genetic basis [heritability out to two generations]
Connection or mechanism between trait and fitness
[early maturation leads to more offspring]
Selection pressure [age-specific predation]
When an evolutionary model demonstrates compatibility with a very broad

set of evidence like this, it is seen as being more strongly confirmed.6
There is, though, another type of variety of evidence to be gained by any
evolutionary model, different from a variety of fit: the variety of evidence consisting
in an accumulation of examples of independent support for aspects of the model.
Variety of Independent Support for Aspects of the Model

Let us turn again to the general outline of a selective model. This time, the
blanks are filled in for the guppies.
Every selection model requires not just a selected trait, but also a claim about
how certain versions or values of that trait are associated with better fitness values.
Thus, independent evidence for this correlation is desirable. In addition, if the
model also has evidence for the existence and strength of the claimed selection
pressure, this lends even more support to the model. Reznick and colleagues
(Reznick and Travis 1996; Endler 1978) checked the mortality rates of the different
populations of guppies and showed that predation was the chief selection pressure.
In addition, to show more directly that predation drives evolutionary selec-
tion and change, Reznick and colleagues took guppies from high-predation
environments and moved them to low-predation environments, and found that
the high-predation guppies evolved the traits of the other population, with
delayed maturity and decreased reproductive effort. All of this provides persua-
sive evidence supporting the “adaptation to mortality model” through independ-
ently and directly supporting its basic assumptions and dynamics rather than
relying solely on successful predictions, which could provide only indirect
support for the model’s assumptions. Such independent confirmation of aspects
of the model often turns out to be the most significant evidence offered for
selection models (Lloyd 1983; 1988/1994).
6
Supported by a technical approach, the Bayesian approach to probability logic; Glymour 1980;
Fitelson 2001.
BOX 1.3 VARIETY OF ROBUST EVIDENCE

More predictions were also confirmed, supporting the causal core of the
selection models.
The cause, higher predation, was also correlated with:
- More frequent reproduction

- Larger litters
- Smaller offspring.
Robustness: Variety of Robust Evidence

Finally, robustness of evidence also plays a key role in supporting these
evolutionary explanations. Reznick and Travis (1996) predicted that the gup-
pies from the high-predation sites would devote a higher percentage of con-
sumed resources to reproduction. This is basically to compensate either for
more of their offspring being eaten by predators, or for the parent guppy having
a lower likelihood of living to breed again. But other predictions also arose from
the theory of the predator-rich environment, including more frequent reproduc-
tion, larger litters, and smaller offspring (see Box 1.3).
Once again, predictions from the model were robustly confirmed by evidence
from the wild. This is an example of distinctly different predictions, involving
different traits, being made using selection theory, and the fit of those predic-
tions with the observational evidence. This is an example of a variety of robust
evidence confirming the model and its causal core (Lloyd 2015b): the higher
predation at the root of selection in the populations. This sort of “model
robustness” has proved significant not just in evolutionary biology but also in
climate science and economics.7
1.2.4 Totality of Types of Evidence Together

The selective model explaining the origin or maintenance of any adaptation is
thus potentially confirmed or supported in a number of different ways by
different kinds of evidence (Box 1.4).
1.3 Summary
Evolutionary adaptation occurs only as a consequence of a natural selection
process; however, selection processes can occur in evolution without producing
engineering adaptations. The evidence needed to document an engineering
7
Lloyd 2015b; Levin 1966; Weisberg 2006; Woodward 2006; Li and O’Loughlin manuscript.
Adaptation 15
BOX 1.4 TYPES OF SUPPORTING EVIDENCE FOR SELECTION MODELS
1. Fit
2. Independent support for aspects of the model
3. Variety of evidence
a. variety of fit
b. variety of independent support
4. Robustness: Variety of robust evidence
adaptation properly in evolution includes not only evidence of a contribution to

fitness of a trait, but also evidence of its heritability and of a past selection process
producing the engineering adaptation. Variations of these requirements occur at
a variety of biological levels of organization, from gene to lineage to combin-
ations of lineages, thus producing adaptations at the full span of biological levels,
as we shall see in Section 2. There are, in addition, a variety of other factors
involved in evolutionary change, which we will also review in Section 2 before
turning our full attention to more theoretical issues involving adaptation.8
In Section 3 we will explore how adaptations are researched in evolutionary
sciences, using a special technique from my philosophy of science work called
the Logic of Research Questions. In learning to apply the Logic of Research
Questions technique, the reader will apply evolutionary theory in context and
learn a variety of evolutionary approaches. In Section 4 we will explore a few case
studies, looking at whether these specific traits should be considered evolutionary
adaptations or not, and how to determine the answer to such a question. We will
look at the evolution of female orgasm, the determination of salamander toe
number, and the evolution of a special genetic mutation in fruit flies. We will also
consider the role and characterization of exaptations, a complementary concept to
adaptation. We will conclude with some reflections on the difficulties of evolu-
tionary exploration. While the subject is challenging, it is also very exciting, and
we have abundant tools to explore the animal, plant, and microbial world.
2 Evolutionary Factors
In this section we consider a large variety of effective factors involved in
evolutionary change that you may not have heard of, including variations on
natural selection such as sexual selection and multilevel or hierarchal selection.
We will explore how the giraffe is built, how human skulls are like snake skulls,
8
Suggested Further Reading: R. C. Lewontin 1978.
and how butterfly wings got their spots, as well as what difference an organism’s
group makes to its evolutionary destiny. While organismic natural selection
may have played a role in these features, it often did not play the most important
role, and that is what interests us in this section. We take these various
evolutionary factors from both traditional evolutionary theory, such as popula-
tion genetics, and newer developments in evolutionary biology, such as evolu-
tionary developmental genetics and beyond.
Our motivation for learning about this variety of evolutionary factors is to
establish a fuller spectrum of causes for evolutionary change that might appear as
legitimate alternatives or supplements to simple natural selection in an evolution-
ary explanation of a trait. As reviewed in Section 1, adaptation explanations appeal
to natural selection as the causal factor. There are, however, many other causal
factors known to have an impact on evolutionary change, most of which can
interact with simple natural selection. Knowing more about these other factors can
help us get a better and more complete picture of how evolutionary change takes
place and can provide a clearer view of how evolutionary researchers might use
these methods. Because we will be concerned primarily with the methods of
natural selection research, we need to know what the alternatives to and variations
of simple organismic natural selection are. We will start with classical population
genetics and some sources of variation from that field.
2.1 Mutation
Genetic mutation is one of the ultimate sources of variety from which natural
selection “chooses” variants in producing adaptive evolutionary change. (This
“choice” is a metaphor for the selectivity of the process.) These mutations can
be big or small in both impact and size, and are well understood in both their
dynamics and components (i.e., DNA and/or RNA).
Mutations vary in how much of the genome they affect. “Point” mutations,
which affect only a single DNA locus or base pair, are the smallest kind; but
they can have large effects, as when the hemoglobin gene is affected in sickle
cell anemia, producing a major disease when occurring in both chromosomes in
an individual. (Note that when this specific point mutation occurs in only one
chromosome, the person with the mutation is protected against malaria, a clear
adaptation to environments with malaria.) We must also note, though, that much
of the genome in multicellular organisms does not code for any protein or gene
product. However, even changes in noncoding regions of DNA or RNA can
affect how genes are expressed, making much of the genome consequential and
subject to natural selection and other evolutionary causes that we will discuss in
this section.
Adaptation 17
There are also structural mutations, which affect multiple DNA base pairs,
from just a few to billions of bases. According to evolutionists Douglas
Futuyma and Mark Kirkpatrick, most structural mutations happen as errors
when chromosomes are replicated, and they include deletions, insertions,
duplications, inversions, reciprocal translocations, and fusions (2017). There
is also whole-genome duplication, which happens more frequently in plants,
many of which are useful in the garden for their toughness, even though they
cannot interbreed.
In any case, all of these genetic mutations comprise the foundation of
variation upon which selection and all other evolutionary causal processes
discussed in this section rest.
2.2 Migration
Another primary way that populations increase their variation is through migra-
tion from other populations with mutations or variants. While one population
may be highly variable through a long history of interbreeding or “outbreeding”
with various other populations, another population may have been relatively
isolated, and hence lack variability from lack of migration from other popula-
tions. These differences in gene flow between populations can affect patterns of
evolutionary change.
Gene flow or migration between populations can be either passive or active.
In many plants, it is passive in that pollen is carried by the wind or by pollinators
to other areas of the world with other populations, as when dandelion seeds and
their parachutes are carried by the wind. In animals, much gene flow or migra-
tion is active.
Futuyma and Kirkpatrick offer the case of the desert locust or grasshopper,
which usually is solitary, but sometimes swarms when conditions become
crowded and resources become scarce (2017). Under crowded conditions, the
grasshoppers’ gene expression changes their shape, hormonal traits, and behav-
ior, and, famously, they swarm in masses of hundreds of millions, flying long
distances in search of better food sources. These activities spread the grasshop-
pers’ genes far beyond their own neighborhood, thus providing a dramatic
instance of genetic migration.
2.3 Drift
Drift has been understood as an original source of population variation from the
earliest work in population genetics, due to Sewall Wright’s studies of small
populations and their random variability based on random sampling from
a larger source population (e.g., Wright 1931). Drift is a classic example of
how a population can fail to evolve an adaptation. The basic idea is that
evolution can result from chance events of survival, reproduction, and inherit-
ance; the resulting process is called genetic drift.
With randomly sorted small populations in a species, the distribution of genes
within the populations varies a great deal. Thus, when one or more of these
small populations becomes extinct, the random distribution of genes into the
populations can “drift,” or change, due simply to the random distributions of
genes in the extinct populations. This leads to nonselective change in the genetic
populations, or genetic drift.
Futuyma and Kirkpatrick show how drift can work with the grove snail,
Cepaea nemoralis, which is famous for its colorful and highly variable shells
(2017). These snails live in pastures that are shared by cattle and sheep, who
often step on the snails accidentally and randomly, independent of their color-
ation. Nevertheless, this random crushing can have consequences for the bal-
ance of colors in later generations of snails; the chance obliteration of some
colors of snails randomly affects the distribution of color genes in future
generations, making this a case of random drift.
2.4 Phyletic Constraint

Consider the role of phyletic history, or as it is usually called, “phyletic inertia,”
due to lack of change from past history. The giraffe’s larynx or voice box is an
intriguing case of how evolution does not often invent new things wholesale. In
other words, evolution usually works as a tinkerer within constraints of the
present design, a principle that is generally accepted and uncontroversial (Jacob
1977). Let’s look at the giraffe’s “design.”
Controlling the larynx is the recurrent laryngeal nerve, and this is true from
fish to mammals in evolution; the same nerve – called a homology (using the
developmental biologists’ conception of homology)9 because it has the same
origin in the genes and cells – appears in development, but it traces different
pathways within the body of different animals because of their dissimilar
development. Evolution never starts from scratch in developing or “designing”
an organism. Remember, evolution is a tinkerer, changing this or that bit of an
organism to make it more suitable or a better fit with its environment in this or
that way, given the parts available to it, and given the developmental and genetic
changes available at a given time to the population.
9
There has been some controversy about the developmental biologists’ conception of homology
because the phylogenetic definition of homology, under which two traits are homologous if they
descend from the same trait in a common ancestor, is more commonly used.
Adaptation 19
For example, in fish, the laryngeal nerve traces within the skull directly from
the brain down to the larynx. Through evolutionary tinkering over time, because
of how mammals evolved from fish and then reptiles, in human beings the nerve
first loops down to the chest and around the aortal arch in the chest, and then
back up to the larynx, which is the long way around. In evolutionary develop-
ment, certain things can change, like the structure of the head, neck, and thorax,
but others cannot, like the nervous system basics, apparently. In other words,
selection acts on existing variation, and the sources of this variation depend on
developmental processes and history.
In the giraffe, the looping of the laryngeal nerve reaches the peak of absurd
shape and development, forcing the nerve to go from the head all the way down
the neck to the chest cavity where the aortal arch is, and then all the way back up
the neck to the larynx. This looping effect, the result of developmental change
within constraints of the present design of the nerves and evolutionary tinkering
over time, makes the nerve about fifteen feet long, and it is thought that this feature
limits the range of vocalizations that giraffes are capable of (Harrison 1981). In
Figure 2.1 Scheme of path of the recurrent laryngeal nerve in Giraffe

camelopardalis.10
10
Wikimedia Commons: Scheme of path of the recurrent laryngeal nerve in Giraffe cameloparda-
lis. Date: February 21, 2010. Created in Inkscape using Oakland_Zoo_dsc_2658.jpg and infor-
mation from R. J. Berry and A. Hallam (eds.), The Collins Encyclopedia of Animal Evolution
(London: Collins, 1986). Author: Dr. Bug (Vladimir V. Medeyko).
certain extinct dinosaurs such as Supersaurus, the laryngeal nerve may have been
up to 100 feet long, and it is believed to have limited their vocalizations as well.
Thus, evolution as a tinkerer, working within the constraints imposed
within a phylum (or large group of related species), can result in traits that
are far from being ideally adaptive to their environment. This is an example
of “phyletic constraint,” in technical terms, within evolutionary biology, and
it is a classic constraint within evolutionary theory on ideal adaptive
engineering.
2.5 Developmental Constraints and the Origin of Evolutionary

Novelty
It might be helpful here to distinguish between innovation and novelty, both of
which are related in different ways to adaptation. Following the distinction
promoted by biologist Günter Wagner (2015), we can think of evolutionary
innovations as referring to novel functional capabilities, like flight or bipedal
walking (Müller and Wagner, 1991; Love 2003, 2006), and evolutionary novel-
ties as structural innovations such as the panda’s thumb. With regard to explain-
ing new functional capacities, “it is necessary to understand how the ancestral
physiological and anatomical substrate for the derived function could be modi-
fied to allow a novel function to arise. These require physiological and bio-
mechanical considerations” (Wagner 2015, p. 76).
In contrast, what is needed for understanding evolutionary novelties, for
example, structural innovations such as the panda’s thumb?
Muller and Wagner write:
DEFINITION: A morphological novelty is a structure that is neither homolo-

gous to any structure in the ancestral species nor homonomous to any other
structure of the same organism . . . Additional bristles are both homologous to
the bristles already present in the source population and homonomous to all other
bristles on the same fly. But there is nothing that can be meaningfully identified
in reptiles with the marsupial bone or in subplacental mammals with the corpus
callosum. (Muller and Wagner, 1991, p. 243)
In such cases the origin of new body parts focuses around the evolution of gene
regulatory networks and differential gene expression. Thus, some evolutionary
explanations focus on the development or embryology of the organism. Darwin
himself called attention to this type of evolutionary explanation in his discus-
sion of the joints of the bones in the skulls – called sutures – in birds and reptiles.
In Figure 2.2, you can see these joints in the skull of a king snake on the left,
and the similar joints or sutures in the skull of a human infant (right). In
Darwin’s time, the joints were thought to be a special adaptation for birth in
Adaptation 21
(a) (b)
Figure 2.2 Snake skull [left] compared with human skull [right]: Note lines
(sutures) in skull. These are places where the bones grow together to form the
complete skull, in both snakes and human beings. Snake skull image credit:
Digimorph, An NSF Digital Library at UT Austin. Human skull image credit:
Mayo Foundation for Medical Education and Research.
mammals, since they made the skull more flexible and compressible to go
through the birth canal.
But Darwin disagreed:
The sutures in the skulls of young mammals have been advanced as

a beautiful adaptation for aiding parturition [birth], and no doubt they facili-
tate or may be indispensable for this act. But, as sutures occur in the skulls of
young birds and reptiles, which have only to escape from a broken egg, we
may infer that this structure has arisen from the laws of growth, and has been
taken advantage of in the parturition of the higher animals. (On the Origin of
Species, p. 197)
In other words, the sutures in the skulls of young mammals may be essential for
helping them squeeze through the birth canal, but this is not their reason for
existence. Rather, the sutures came into existence because of the necessities of
development, going all the way back to the reptiles, and the uses to which the
sutures are later put by evolution are bonus side effects.
For a related evolutionary challenge, consider the problem of why male
mammals have nipples. Nipples clearly provide a reproductive advantage to
female mammals in that they ensure reproductive success by providing the
means to feed the offspring. But there is no known contribution to fitness for
the males.
The evolutionary explanation for the existence of male nipples is based on the
development of the embryo. Males and females share the same embryological
form at the beginnings of life – they start off with the same basic body plan, and
only if the (chromosomally male) embryos receive a jolt of hormones during the
eighth week of pregnancy do any sexually distinguishing characteristics appear.
There may also be a role for specifically female hormones and developmental
cues, but we haven’t established any yet.
In females, nipples are adaptations – they were actively selected for – but
the males get them for free. But there have been problems getting this kind
of evolutionary explanation accepted, for a variety of reasons. We will
discuss this type of example further in Section 4, in the case of the female
orgasm.
Another interesting case of developmental explanations arises in the
explanation of why so many miniaturized salamanders have only four toes
instead of the usual five toes of land animals. There are numerous lineages in
which the salamanders become miniaturized, or dwarfed, and in all of those
lineages, the miniaturized forms converge on having only four toes on their
rear legs instead of the five toes of the usual-sized salamanders and other land
animals and four-legged creatures, such as you can see in Figure 2.3 of the
independent lineages.
Why so? Is selection driving this toe reduction, so that all lineages are
under selection when tiny to produce the four-toed form? So that there is
a functional or adaptive advantage in every lineage to having only four toes
in the available environments, and this selective pressure is expressed in
every lineage? Or is there another, more form-based evolutionary explan-
ation, where only limited developmental and structural options exist in the
lineages, and once miniaturization happens, only the four-toed forms are
really available? Actually, these explanations are complementary and are
likely best combined, according to Wake.11 This case is discussed further in
Section 4.2.
Another important place for development is in the origin of developmental
novelty. For example, in the case of the evolution of the eyespots on butterfly
wings, which are relatively recent novelties or innovations on the wing color-
ation of butterflies, they are understood to be adaptive for avoiding predators
through camouflage. In order to tell their full evolutionary story, we need
evolutionary developmental biology to tell us where the novelty originated,
which we can learn from the developmental genetics of butterflies and related
organisms (Wagner 2000, p. 96).
11
See discussion by Griesemer 2013, 2015.
Adaptation 23
Figure 2.3 Independent four-toed lineages in the salamander family

Plethodontidae. Independent evolution of four-toed state in three separate
lineages. (Wake 1991, p. 548, Figure 1).
It turns out that eyespots are completely unique to butterflies, so they are
genuine evolutionary novelties. The genetics show that they are induced genet-
ically by a small group of cells called the “eyespot organizer,” so the evolution-
ists concluded that the key evolutionary step occurred in the origin of this
organizer (Nijhout 1991). Butterflies and fruitflies are from the same assem-
blage, Panorpida, within the superorder of insects, Endopterygota (Song et al.
2018). (The interested reader can check out a visual depiction of their relation
on the web, for example, Wikipedia.)
So, the evolutionary developmental geneticists studied the genes in fruit fly
wing development and how the same genes were involved in butterfly wing
development. Except for butterfly wings, the genes had acquired a new func-
tion, an innovation. They then determined exactly the two genetic modification
events that were required to result in the eyespot organizers. This knowledge
about the evolutionary novelty requires detailed knowledge of both fruit fly and
butterfly wing development. And the genetic architecture of butterfly pigment
patterns “radically changes as a consequence of the origin of eyespots” (Wagner
2000, p. 97).
What this means is that any regular population genetics model of evolution by
natural selection and other forces of these butterflies would not be effective,
because the entire range of possibilities of the model would be incorrect; it
would be transformed by the evolution of the novel eyespots. After the
evolutionary innovation, we need a new coordinate system – a new set of

possibilities – to model the variation of the system.12 And Günter Wagner spells
out the implications of this fact:
after the emergence of an evolutionary innovation, we need a new coordinate

system to describe the variation of the system (Shpak and Wagner, 2000) .. . .
it is essential to include developmental mechanisms in the explanation of
evolutionary innovations. By implication this is also the reason why devel-
opmental evolution makes an indispensable contribution to evolutionary
biology. (2000, p. 97)
In other words, Wagner emphasizes the importance of including the evolution of

developmental systems in any story of the development of evolutionary innov-
ation such as that involving the butterfly eyespots. Once we have a space of
possibilities that includes evolutionary development, we have a more complete
evolutionary theory.
2.6 Genetic Linkage

Genetic linkage means that genes are being inherited together at a higher rate than
random. They are another illustration of developmental constraint or forces of
cellular structure and development making a difference to evolutionary change.
Because of genetic linkage, adaptation may be constrained, due to a lack of
genetic variation for selection to act on. With less genetic variation for selection to
act on, adaptation will have a more restricted array of adaptive traits from which
to choose, thus limiting the level of adaptation in the organisms’ population.
Human genes are lined up on two sets of chromosomes. When two alleles
(versions of a particular gene) are close together on a given chromosome, they
are more likely than not to be inherited together during the processes of
reproduction, a phenomenon called “genetic linkage.” During meiosis, the
chromosomes cross over, and some material from the mother’s chromosome
mixes with some material from the father’s chromosome. The further apart the
alleles are on each chromosome, the more likely it is that they will be separated,
and not linked, during meiosis and reproduction.
Most such genetically linked genetic traits are either closely spaced together
on a single chromosome, or they govern a common pathway. We can discover
which genes are linked by comparing genetically crossed plants’ or animals’
genes to calculate the recombination frequency, which measures how often the
genes change position. Two genes that are very close together will have few
recombination events and therefore a low recombination frequency.
12
Shpak and Wagner 2000.
Adaptation 25
By finding recombination frequencies for the various gene pairs, we can

create linkage maps that show the order and relative distances of the genes on
the chromosomes. This is how the human genome was first mapped and its
DNA was sequenced.
2.7 Pleiotropy
Pleiotropy occurs when single genes have multiple phenotypic effects or traits.
The originator of genetics, Gregor Mendel, conducted pea studies that revealed
pea plants with pleiotropy – genes that had more than one trait associated with
them. For example, the plants with colored seed coats always had colored
flowers and colored leaf axils (the part that attaches leaves to stems). The
opposite was true of colorless seed coats, which had white flowers and no
pigment on their axils. Mendel’s findings were later confirmed to be the results
of single genes for these multiple traits.13
We are familiar with pleiotropy in white cats with blue eyes, 40 percent of
whom are also deaf. It turns out that pigmentation plays a role in maintaining
fluid in ear canals, without which there is deafness (Sunquist, 2006). This is
a common case of pleiotropy, and even works partway, in that a cat with one
blue eye and one yellow eye is deaf only on the blue-eyed side of its head.
Thus, features or traits of genes can appear that are not separately selected
for – they just come along for the ride. In the case of the peas, these may be
benign traits, but in the case of deafness, they can be maladaptive, even though
the white fur and blue eyes themselves may be prized by certain cat owners. The
crucial point is that we cannot infer that every trait is an adaptation, selected by
natural selection for its current state or value; it may be a ride-along trait of
pleiotropic genes.
2.8 Cultural Coevolution Factors

For processes like cultural selection, our best example may be the gene-cultural
coevolution of lactose intolerance, or the adult inability to digest milk (Feldman
and Cavalli-Sforza, 1985). The basic idea is that culture can shape biological
evolution. Dual inheritance theories of genes and cultural inheritance not only
track two different types of inheritance but can also represent their dynamic
feedbacks when it occurs.
Feldman and Cavalli-Sforza initiated gene-culture evolutionary models in
1973, when they introduced a model that incorporated cultural transmission (see
also Feldman and Cavalli-Sforza 1981). The evolution of lactose absorption
13
Fairbanks and Rytting 2001.
represents a good example of gene-culture coevolution. There is systematic

variation in adult humans’ ability to digest milk. In fact, most adult humans
cannot digest it, and their lack of lactase, the enzyme that breaks down milk
sugar, lactose, means that when they drink milk, they are likely to get stomach-
ache, nausea, and diarrhea. There is a genetic basis to the differences between
people in their ability to drink milk and eat milk products, based on a dominant
genetic trait, and this genetic difference correlates to the history of dairy
farming in the relevant populations and their cultures. In cultures with dairy
farming, over 90 percent of the population’s adults usually can digest milk,
while in nondairy farming cultures, the rate is less than 20 percent. It is believed
that, since dairy has been an important part of the diets of some human groups
for over 6,000 years, such cultural practices may have set up a selective regime
under which the allele for lactase selection was favored.
Feldman and Cavalli-Sforza (1985), following work by Aoki (1984;1986),
used gene-culture coevolutionary theory to investigate the evolution of lactose
absorption. They modeled lactose absorption with differential cultural trans-
mission of milk usage. Their analysis found that whether or not the allele for
milk absorption was favored depended crucially on the likelihood that the
children of milk users become milk users themselves, in other words, whether
they continued the cultural practices of their parents. Thus, the cultural practices
and processes complicated the selection process, often to the extent that the
outcome changed from the one expected under purely genetic results. Thus,
gene-culture coevolutionary models can be very informative, and interesting
results can explain a variety of outcomes in human society.14
2.9 Niche Construction

Lewontin (1983) proposed that biological evolution depends on “niche con-
struction,” as well as natural selection and inheritance. The notion of niche
construction has been developed since then by Kevin Laland, John Odling-
Smee, and Marcus Feldman into a theory about the activities, choices, and
metabolic processes of organisms, “through which they define, choose, modify,
and partly create their own niches” (2000, p. 132). We can see this when
organisms choose their own habitats, their own mates, and then also choose
resources and construct important parts of the local environments, for example,
webs, nests, or burrows, but also chemical environments.
Organisms also partly destroy their own habitats by stripping them of
resources or building up waste. Niche construction can interact with natural
selection in interesting ways. For example, organisms can counteract natural
14
Feldman and Laland 1996, p. 454. See also Boyd and Richerson 2009.
Adaptation 27
selection by digging burrows that protect them from the cold. On the other hand,
they may provoke natural selection through niche selection choice of a new food
source, subsequently selecting for a new digestive enzyme. Or they might do
both, for example, when building a nest protects an organism but also estab-
lishes a novel selection pressure by acting on a second trait for defending the
nest. In each case, though,
[N]iche construction modifies one or more sources of natural selection

in a population’s environment and, in so doing, generates a form of
feedback in evolution that is not yet fully appreciated. (Laland et al.
2000, p. 133)
This feedback generated through niche construction constitutes the primary

evolutionary significance of niche construction. Many organisms modify the
selection pressures on themselves through niche construction, and these selec-
tion-altering traits coevolve with traits whose fitness depends on changeable
sources of selection in environments. For example, take the beavers’ niche
construction activity of building a dam. The dam itself sets up a variety of
selection pressures on the beavers, and these pressures feed back to act on the
genes responsible for the dam. Take the traits such as the details of the teeth that
must cut down the trees to make the dam, the tail as a balancing and warning
tool, the feeding behavior that is changed through having a dam, and the social
system once the dam is set up – all of the genes for these traits are under different
selective regimes once the dam exists. Also, the dam will affect many future
generations of beavers that inherit the dam and the altered stream, which is now
a pond, and a source of many sources of food and shelter. The feedbacks
produced by the simple existence of the niche alteration of the dam are enor-
mous for evolution.
And that’s just one example. Think of ants who build their nests, compli-
cated structures around which they move their broods of eggs, or think of
bees, who build hives with similar complexity and defenses. There is strong
evidence that the burrow or nest came first, and the subsequent defenses and
elaborations evolved later, building on top of the initial move in niche
construction.
2.10 Sexual Selection

Darwin (1859, 1871) proposed the mechanism of sexual selection to explain
evolution of conspicuous traits in males that reduce their survival, such as bright
plumage and vigorous courtship displays. Christopher Murphy defines sexual
selection as “differential mating success produced by variation among members
of one sex in a trait that affects competition for mates” (1998, p. 8).
Darwin defined two major types of sexual section:
[I]n the one it is between the individuals of the same sex, generally the male sex,
in order to drive away or kill their rivals, the females remaining passive; whilst
in the other, the struggle is likewise between the individuals of the same sex, in
order to excite or charm those of the opposite sex, generally the females, which
no longer remain passive, but select the more agreeable partners. (1871, p. 398)
Subsequent discussions of sexual selection have focused on these two types of

sexual selection, male–male competition and female (mate) choice. A number
of theorists have suggested additional mechanisms, and Murphy has general-
ized that traits can be subjected to sexual selection “even if they do not affect the
outcome” of selection between individuals of the same sex or different sexes,
that is, they are totally independent (1998, p. 16).
He distinguishes two types of sexual selection based on whether variance in
mating success is the result of “trait-dependent outcomes of interactions between”
individuals of the same species (1998, p. 9). He uses this distinction to construct
a framework for classifying different types of sexual selection previously proposed.
Lynda Delph and Tia-Lynn Ashman (2006), Steve Arnold (1994), and Delph
and Christopher Herlihy (2012) distinguish selection for survival (or viability),
for mating success (or sexual selection), and fecundity (or fertility selection),
and how they act within each sex to determine the evolution of sexual dimorph-
ism —or differences in form in the different sexes— in Silene latifolia,
a wildflower common in North America. Delph and Herlihy experimented on
Silene by varying distinct selection regimes that differed in flower size,
a sexually selected trait. In Silene, flower size and number trade off within
each sex, depending on the selection pressures. And males produce more
numerous and smaller flowers than females.
The outcomes of the selection experiments that placed the different varieties
of selection pressures on the plants were as follows. Fecundity selection favored
males with high flower production, since it was correlated with pollen produc-
tion, key to success in fecundity. Also, viability success opposed success in
sexual selection, favoring males from the large-flower lineage. But in females,
fecundity and viability selection operated in the same direction, favoring those
with greater seed production and survival, which were also those from the large-
flower lineage (Delph and Herlihy 2012). Thus, these three types of selection
can interact in a variety of ways to produce evolutionary outcomes.
We also see sexual selection acting versus viability selection on size in the
marine iguana in the Galapagos Islands in an unusual way, as they adapt to El
Niño temperature changes in their environment, in a study by Martin Wikelski
and Corinna Thom (2000).
Adaptation 29
Changes in bone metabolism allow these lizards to reversibly alter their

length as adults in a mechanism unknown in other vertebrates. In two long-
term studies of two iguana populations, one of 18 years and one of 8 years, the
lizards shrank by as much as 20 percent when exposed to severe food shortages
brought on by El Niño conditions. When La Niña conditions resumed, the alga
food sources were renewed, and the adult iguanas resumed their previous
lengths. The iguanas that shrank more survived longer than the larger iguanas
and were able to feed more. Larger individuals shrank more than smaller ones,
and females shrank more than males of the same size. This was believed to be
because they exported their energy into clutches of eggs in the year before an El
Niño.15 This shrinkage, of up to 20 percent, is mostly due to bone absorption,
caused by energetic stress and low food availability.
2.11 Multiple Levels of Selection

It is important to realize that evolutionary adaptations can occur at many levels
of biologic organization, including the genic, cellular, organismic, family,
demic, lineage, and mutualist/holobiont levels.
2.11.1 Genic and Cellular Levels

At the genic level, we have cases of meiotic drive, wherein sperm cells possess the
means to kill off competing sperm cells in a manner that favors inheritance of
their own genes, for example, in the t-allele in the house mouse (Lewontin and
Dunn 1960). The t-allele causes sterility in the male mice it appears in, and demes
or groups in which the t-allele is more common clearly have a disadvantage in
reproduction. Still, the t-allele persists in the population because it outcompetes
other sperm cells at the genic level within gametic reproduction, even though it is
selected against at the two higher levels of selection.
On the cellular level, we have the cooptation of eukaryotic (nucleus-
containing) cells by free-living bacterial mitochondria, wherein we understand
the previously independently living prokaryotic (non–nucleus-containing)
mitochondria have been coopted and absorbed cooperatively and symbiotically
into the eukaryotic cell (Margulis [AKA Sagan] 1967)). The new eukaryotic cell
reproduces both its own DNA and the DNA of the mitochondria in parallel.
2.11.2 Symbiosis Level
These mitochondria are early cases of holobionts, where two independent sets of
organismic genomes are linked together through coadaptation and coevolutionary
15
Wikelski, Carrillo, and Trillmich 1997.
change. Other examples occur with animals and their gut microbiomes (commu-
nities of microbes), such as cows and the bacteria, viruses, and fungi that they
depend on to digest the cellulose in their diet; similarly for termites, who require
their gut microbiome to digest the wood fibers in their diet. There are adaptations
that can emerge at the coadaptive level, such as the pedestals built by dung beetles
on which they deposit their eggs. When the eggs hatch, they are surrounded by the
dung, which contains the gut microbiome that will allow them to thrive in their
environments (Lloyd and Wade 2019; Suárez and Triviño 2020; but see Douglas
and Werren 2016).
The building of the pedestals made of dung is a joint adaptation of the
mutualistic holobiont itself, serving its shared, joint (epistatic) fitness compo-
nent, as modeled by Lloyd and Wade (2019) and as theorized as a “manifester of
adaptation” by Suárez and Triviño (2020; see Lloyd 2017).16 While we model
such a holobiont as a sort of community or group, let us now consider a more
general group-level approach.
2.11.3 Group Level
Consider a group selection case from Michael Wade and community selection
case from Charles Goodnight. In the group selection case we must consider
genetic interaction, that is, the fact that individual genes’ selective fitnesses are
never considered additively in the system, but always in relation and interaction
with the other genes in the system, including genes of other organisms in the
same social group or family as the original organism.17
Wade offers two card games to help understand what is going on in group
selection like this. Take the card game of War, wherein each player lays down
a card at each play, and the highest card wins. The cards are totally independent,
and there are no interactions with the other cards in the deck. In poker, however,
the value of each card depends very much on what other cards you hold in your
hand. “Interactions are the essence of poker . . . .[it has] many possible winning
hands, depending on the combinations of cards, the spatial and temporal order in
which hands are played, the abilities of the other players in the game, and the
past history of hands played by the ‘population’ of players” (Wade 2016,
p. 190).
There is much evidence for the effectiveness and power of group selection as
defined by Wade and Goodnight, both in the laboratory and in the wild. Group
16
This means that there may be a component of fitness of the mutualistic combination of organ-
isms, or a shared epistatic component of fitness (Lloyd and Wade 2019).
17
Wade 2016, p. 188.
Adaptation 31
selection can produce group adaptive and behavioral changes that allow the
group to thrive in otherwise inhospitable conditions.
While many of those taking a genic approach are unaware of the power of
group selection, this does not change the status of the empirical evidence nor the
likely efficacy of group selection in producing evolutionary change in popula-
tions and species in the wild (see Lloyd 2005b)18. One of the most striking
examples of the success and power of group selection is in the domestic
chicken. Chicken breeders had long selected for even tiny improvements in egg-
laying rates of hens under domestication, but had not measurably improved
their rates due to conflict among the hens in captivity, and their high mortality
rate. Group selection on the hens for hen groups that got along better and were
more docile, the “kinder, gentler” hens, improved the egg-laying productivity of
the hens by up to 60 percent (Cheng and Muir 2005), thus demonstrating the
adaptive power of group selection regimes.
Sometimes when multiple levels of selection are understood to occur simul-
taneously, this is referred to as “hierarchical selection.” For the classical mod-
eling of such systems, see Sewall Wright (1931), or for its first real-world
instantiation, see Lewontin and Dunn’s work on the house mouse with its
t-allele (1960).
2.11.4 Lineage Level
Lineage levels of selection may also be effective in producing evolutionary

change, at the very least, under the description of product-of-selection adapta-
tions rather than engineering adaptations (see Section 1). Consider, for example,
the rates at which lineages speciate, that is, the rate at which they form and
branch off new species. This rate varies among different lineages, and interest-
ingly, it varies with the geographic distribution of the species, that is, how the
lineage ranges over the Earth, and how it occupies different sectors or areas of
the Earth’s geography.
Elisabeth A. Lloyd and Stephen Jay Gould (1993) followed the line of thought
that lineages of gastropods might develop higher speciation rates depending on
their breeding mechanisms, and may also vary in their long-term species survival
rates. Those lineages that reproduced in such a way that the young of the species
were sedentary and attached themselves to rocks at the beginning of life, thus
limiting their range very sharply, were seen as more likely to speciate. The
18
Against a conventionalist interpretation of genic selectionism, à la Sterelny and Kitcher (1988)
or Kerr and Godfrey-Smith (2002), see Lloyd (2005b) and Lloyd, Lewontin, and Feldman
(2008), showing its undesirability and the nonequivalence of the claimed group and genic
models.
lineages that reproduced by having the young float freely in the seawater were
able to travel far from their place of birth and cover a greater geographical range,
and were seen as less likely to speciate. Later, the lineage-level adaptive trait of
geographic range of offspring in both gastropods and mollusks was found to be
correlated with the long-term species survival rate (Jablonski and Hunt 2006;
Jablonski 2008). This accorded well with the Lloyd and Gould theory of species
selection, which does not require engineering adaptations at the species level, but
finds product-of-selection adaptations nonetheless.
2.12 Evolutionary Mismatch

Evolutionary “mismatch” is a state of disequilibrium, “whereby a trait that
evolved in one environment becomes maladaptive in another environment.
Mismatch is an integral part of evolution in changing environments and is
becoming increasingly common for all species living in human-altered envir-
onments” (Lloyd, Wilson, and Sober, 2011). In a classic case of mismatch,
a trait that is adaptive in an ancestral environment becomes maladaptive in
a modern environment, or ill-suited to perform its function. The situation can
typically only be addressed by a behavioral accommodation, subsequent evolu-
tion, or another environmental change.
Take baby sea turtles, who have adapted to move toward the light of the moon
reflecting off the sea as soon as they hatch on the beach, an adaptation that leads
them immediately toward the ocean. Once beach houses, with their deck lights
are built, however, the baby sea turtles become confused and disoriented,
moving further inland toward the beach houses and away from the ocean,
which is maladaptive, a case of evolutionary mismatch. The originally adaptive
trait of moving toward light has now become maladaptive in this new, modern,
beach-house environment. The solution for protecting the sea turtles is to build
walls to contain the light within the boundaries of beach-house properties, thus
allowing them to react to natural light and move once again toward the ocean.
Evidence for evolutionary mismatch or maladaptations follows the same
route as that for adaptations, differing primarily in the extra step involving
a link between fitness and the trait, and its environment of selection. In evolu-
tionary mismatch or maladaptations, the new link requires evidence for a past
link between fitness and the trait, along with evidence for a present negative link
(e.g., linking the turtles’ maladaptive behavior with the new beach-house
environment). The literature about mismatch holds various views about whether
an actual negative fitness value is required; some require only damage to well-
being (e.g., cancer or diabetes onset that can occur after reproductive age).
But all the usual assumptions and steps in providing evidence for an adapta-
tion need to be filled in. Thus, an adaptive explanation for a trait is not confirmed
Adaptation 33
BOX 2.1 EVOLUTIONARY MISMATCH MODEL AND CONFIRMING EVIDENCE
population [______]
trait(s) [______]
genetic basis [______]
past positive or neutral connection or mechanism between trait(s) and
fitness [______]
past selection pressure or environment [______]
present negative connection or mechanism between trait(s) and fitness
[______]
present selection pressure or environment [______]
primarily by providing a story or prediction that says that it would be good for
an organism to possess the trait in question, but rather by a variety of detailed
biological measures and assumptions. We can see how Box 2.1 would be filled
in for the sea turtle case, with the present negative connection between trait and
fitness being the death of baby sea turtles who climb up the beach toward the
beach houses, and the present selection pressure being the presence of beach-
house lights attracting the baby sea turtles.
2.13 Summary
Evolutionary adaptation occurs only as a consequence of a natural selection
process; however, selection processes can fail to produce engineering adapta-
tions. The evidence needed to document an engineering adaptation in evolution
includes evidence not only of a contribution to fitness of a trait, but also of its
heritability, and of a past selection process producing the engineering adapta-
tion. Variations of these requirements occur at a variety of biological levels of
organization, from gene to group to lineage to combinations of lineages, thus
producing adaptations at the full span of biological levels. In this section we
have given a whirlwind review of a variety of factors that play roles in
evolutionary change over time.19
I have reviewed a variety of ways in which organisms can evolve, with
a variety of selective and nonselective causes producing these outcomes. As
I hope the reader can see by now, evolutionary research is complicated by the
presence of this full variety of evolutionary factors, because any one or
19
Suggested Further Reading:
Harrison (1980); Inside Nature’s Giants | PBS www.pbs.org/show/inside-natures-giants/;
Marshall Cavendish Corporation (2010) Mammal Anatomy: An Illustrated Guide.
a combination of them might be at stake in a given case of evolutionary change.

We cannot simply assume that evolutionary adaptation is occurring at the
simple level of the organism in a simple selection process in a given system.
This fact has consequences for how we do evolutionary research and the
research questions we ask, as we shall see in the upcoming sections.
3 Adaptationism and the Logic of Research Questions

3.1 Introduction
In “The Spandrels of San Marco and the Panglossian Paradigm,” Stephen Jay
Gould and Richard C. Lewontin (1979) drew attention to several risks of using
an evolutionary research method that they called “adaptationism.” They drew
attention first to two weaknesses of adaptationism:
[1]We would not object so strenuously to the adaptationist programme if its

invocation, in any particular case, could lead in principle to its rejection for
want of evidence. We might still view it as restrictive and object to its status as
an argument of first choice. But if it could be dismissed after failing some
explicit test, then alternatives would get their chance. Unfortunately,
a common procedure among evolutionists does not allow such definable
rejection . . . [2] The criteria for acceptance of a story are so loose that
many pass without proper confirmation. Often, evolutionists use consistency
with natural selection as the sole criterion and consider their work done when
they concoct a plausible story. But plausible stories can always be told.
(Gould and Lewontin 1979, pp. 587–88)
Note here that in the first complaint, Gould and Lewontin are asking for
a “stopping rule” of some kind that would signal the abandonment of the search
for adaptive stories, or the time to investigate alternative accounts from the
evolutionary canon.
The biggest danger they emphasized (issue [2] above) may be summed up
briefly as the risk of what they called “just-so stories” serving in place of well-
confirmed adaptive explanations. What happens in such cases is that the biolo-
gist’s imagination serves her well for producing selective accounts for what are
assumed to be adaptive traits, but that such accounts are not carefully examined
for their empirical support, according to the standards described in Section 1.
Instead, the biologist’s good storytelling ability substitutes for evidence in
support of the adaptive account, and such “just-so stories” are accepted on the
basis of their plausibility rather than firm evidential support for a variety of
independent aspects of the model (see Section 1). In such cases, a variety of
good evidence is neither sought nor provided; and the evolutionary basis of such
traits is simply assumed and granted without firm evidential support – it is based on
Adaptation 35
the attractiveness and plausibility of the conclusion or prediction of the evolution-

ary model.
A third problem clarified by Gould and Lewontin with adaptationism, as
practiced in the manner they opposed, was the standard of assuming that selection
was the only or the main evolutionary factor operating on a trait, thus neglecting
the presence of the other evolutionary factors that we reviewed in Section 2, such
as pleiotropy, phyletic inertia, and so on. These other factors, summed up as
“evolutionary factors,” are universally accepted as possible contributors to evolu-
tionary change by every practicing evolutionary theorist but are often not con-
sidered as really “in the running” for actual explanations, complained Gould and
Lewontin, and were given only “lip service.” This meant, that even though these
other evolutionary factors were recognized as technically possible, they were
never acknowledged as real possibilities of evolutionary change, which they
thought was a scientific error.
In this section, I present a framework for analysis that makes such “methodo-
logical adaptationism” and other ways to approach evolutionary research clearer.
Before we proceed, let us consider some definitional issues. Notably, there
are other types of adaptationism, as highlighted by philosophers Peter Godfrey-
Smith (2001) and Tim Lewens (2009). For example, there is empirical adapta-
tionism, which emphasizes the predictive and explanatory benefits of the role of
natural selection in evolutionary processes, and there is explanatory adapta-
tionism, which claims that natural selection “has unique explanatory importance
among evolutionary factors” (Godfrey-Smith 2001, p. 336). However, here I am
concerned with methodological adaptationism understood as the view that “the
best way for scientists to approach biological systems is to look for features of
adaptation and good design” (Godfrey-Smith 2001, p. 337).
My focus is on subfields of evolutionary biology that rely on this approach in
their day-to-day research, such as behavioral ecology, sociobiology, evolution-
ary psychology, and some branches of genetics, although it occasionally pops
up elsewhere. In Section 4, I expand on the risks methodological adaptationism
poses to scientific reasoning in evolutionary biology. Also, I emphasize that
I am not attacking the notion of looking for adaptations in evolutionary studies:
I am not anti-adaptation. The issues concern which framework of research
questions is most appropriate and fruitful in any given case. But first, we must
understand methodological adaptationism as a research program.
3.2 The Logic of Research Questions

As reviewed in the preceding sections, there are a variety of evolutionary factors
that can influence the form and distribution of a given trait in a population or
species. While natural selection at a variety of levels may be the most significant
factor, we also have genetic linkage, phyletic history, developmental factors,
embryological constraints, and social and niche coevolutionary factors, and,
I would add, drift, mutation, chance, and migration, or combinations of any of
these processes in a correlated or linked trait, among other causal and explana-
tory factors.
I call this basic approach using the full variety of evolutionary factors we’ve
discussed the evolutionary factors framework of evolutionary theory; its
fundamental research question is: “What evolutionary factors account for
the form and distribution of this trait?” Sometimes, several of these factors
operate simultaneously on a given trait, but often only one or two are the major
factors causing its form and distribution at a given time.
When we investigate the evolutionary account of a given trait, in the fields
we’re discussing (i.e., evolutionary psychology, behavioral ecology, and socio-
biology), it is usual to prioritize the functional factors, natural selection and
sexual selection, as the most significant ones in evolutionary research. We might
start with the question:
“Does this Trait Have a Function?”20
If the trait, after investigation, does not appear to have a correlation with
fitness,21 or does not appear to have evidence of design – hence, does not appear
to have a current or past function – we pursue other possible evolutionary
explanations, such as whether it might be due to genetic linkage with another
trait or a by-product of selection (i.e., indirect selection). Alternatively, it may
be present due to developmental or embryological constraints, or phyletic
inertia, and so on. Pursuit of such explanations consists of testing them against
available evidence and searching for new evidence specific to those factors.
However, the approach dominant among leading animal behaviorists, behav-
ioral ecologists, many human evolutionists, and nearly all evolutionary psych-
ologists (who ask evolutionary questions to analyze psychological traits), is the
one described above (section 3.1), called methodological adaptationism.
Under this approach, the leading research question is: “What is the function
of this trait?” And the research consists of a search for supportive evidence for
adaptive hypotheses that can explain the trait’s presence in the population.
20
See Rose and Lauder (1996) and Martins (2000) for examples and methodological details. Note
that leading with this specific research question does not describe research in evolutionary
developmental biology, which starts with nonfunctional questions in evolutionary developmen-
tal biology and leads with questions concerning form and structure.
21
Symons gives reasons against using correlation with fitness for detecting adaptations and prefers
evidence of design (1990).
Adaptation 37
Issues about method in behavioral ecology and biology revolve around

evolutionary adaptations, one of evolution’s biggest successes.22 I take it as
given that our living world is filled with such adaptations.
Let us examine a defense of an “adaptationist research program” by one of
modern evolutionary theory’s founders, Ernst Mayr, written in reaction to
Gould and Lewontin’s “Spandrels” paper. Mayr sets up the problem so that
selection is the only positive answer to the evolutionary question. He writes:
The adaptationist question, “What is the function of a given structure or

organ?” has been for centuries the basis for every advance in physiology. If
it had not been for the adaptationist program, we probably would still not yet
know the functions of thymus, spleen, pituitary, and pineal. (1983 p. 328;
emphasis added)
Mayr offers the discovery of the lateral line in fish – the complex dark line
running along the sides of nearly all fish – as an example of the power of the
function question; if we had just let the line remain mysterious, we would never
have understood its function as an additional sense-organ in the life of fish.23
Moreover, Mayr defends the adaptationist program as harmless, when applied
correctly:
The question whether or not the adaptationist program ought to be abandoned

because of presumptive faults can now be answered. It would seem obvious
that little is wrong with the adaptationist program as such, contrary to what is
claimed by Gould and Lewontin, but that it should not be applied in an
exclusively atomistic manner. (1983, p. 332)
Mayr’s approach to adaptationism is widely adopted among evolutionary

psychologists, behavioral biologists, and evolutionary ecologists alike.
Thus, identifying the function of a trait is the primary aim of the adaptationist
program, which also aims to identify the formative selective pressures. Note
that identifying a trait’s function is not necessarily to identify its selection
pressure: commonly, for example, we can have multilevel selection, and there
are multiple processes responsible for the trait’s form and function. The trait
itself does not tell us how to describe its selection pressure, although the
investigating biologist may play favorites about which process to privilege in
their explanations.24
Note also that a trait having utility now is not the same as having
a “function” in the selective sense. For example, a trait could contribute to
22
See Lewens (2009) for nine types of adaptationism. Amundson (2001) and Sansom (2003) have
also emphasized the multiple nature of adaptationist questions and answers, but not in the way
I do here.
23 24
See Williams 1966, pp. 10–11. For examples, see Wade 2016.
fitness in the current population without having been formed by selection to do

so. Gould and Elisabeth Vrba (1982) dubbed such traits “exaptations”; these
have current utility, or “effects,” but not functions in the selective or engineer-
ing sense. Evolutionary psychologists and behavioral biologists don’t often
use this former category of evolutionary outcome, even when appropriate (see
Section 4.4).
Alternately, a trait could have had a function in the past, and a correlation
with fitness then, and be a “past adaptation,” with no evolutionary function now,
or even be an evolutionary “mismatch” now. Again, human and behavioral
evolutionists rarely assign traits to past adaptation, and usually claim current
fitness benefits.
While the adaptationist approach may look biased on its face, since it
starts with the assumption that the trait is an adaptation rather than one
of the other possible features, this assumption is supposed to be only
temporary. If it turns out that the trait does not appear to have a function,
then the biologist is supposed to move on to other possibilities. This
supposedly benign program has been advocated by many biologists since
Mayr.
Thus, the methodological adaptationist approach is seen as the “most helpful
way to proceed”: look for selective explanation in every case, which upon
failure of the selective explanations might lead you to nonselective explan-
ations, which could then be pursued if that is where evidence led (Godfrey-
Smith 2001, p. 342). Adaptations are most often indicated by their “specificity,
proficiency, precision, efficiency, economy, complexity of design, reliable pro-
duction, costliness, etc.” (Andrews et al. 2002a, p. 503 [from Williams 1966]).
Optimality models, discussed in Section 1, can be used to investigate these
features.
But it is still an open question whether the method outlined here in practice
allows nonadaptive explanations to ever win the day. Remember that this issue
of “lip service” was a key concern in Gould and Lewontin (1979). Do
researchers in fact find themselves willing to embrace nonadaptive explanations
when the evidence points away from adaptation? Other evolutionary factors are
often explanatory, but are they appealed to when necessary under the methodo-
logical adaptationist approach?
I use what I call the Logic of Research Questions to help unpack and highlight
the differences between the relevant theoretical approaches. The logic of the
research questions we ask constrains what classes of answers we can give that
are responsive and relevant.
Crucially, research questions carry with them an appropriate, unique class of
possible and responsive answers, distinct from other contrasting classes of
Adaptation 39
BOX 3.1 “WHAT IS THE FUNCTION OF THIS TRAIT?”

There are many possible and responsive answers to such a research
question, all of which take the common form:
Possible and Responsive Answers
A: The function of this trait is F.

A: The function of this trait is G.
Etc.
answers. We need to think very hard about the research questions we ask and the
answers they allow, because the questions can lead us to miss what’s really
going on, and therefore to scientific failure. While I apply this logic to the
adaptationist methodology, it can be applied to any scientific investigation; the
logic of research questions is applicable to any scientific field that experiences
controversy about methods and inference.
The methodological adaptationist asks, echoing Mayr,
Someone following the evolutionary factors framework asks, on the other
hand, quite generally:
We can now see a clear logical contrast between the two distinct frameworks and
their corresponding sets of research questions and possible responsive answers.
Note that the first answer following the general question, “What evolutionary
factors account for the form and distribution of this trait?”, specifically, “Does
this trait have a function?”, is an adaptation answer, which was done to suggest
that, pragmatically, in the fields of evolution we’re examining, adaptation also is
explored, as a priority, in the evolutionary factors methodology. This does not
necessarily follow from the evolutionary factors logic, but it is a priority for
those in the named fields of study because of their research interests, which
center around functions.
But under the evolutionary factors approach, the key question about adapta-
tion is: “Does this trait have a function?” which is logically very different
from the key question asked by the methodological adaptationist. Here, there is
no assumption that the trait is an adaptation, in sharp contrast to leading
research with the question: “What is the function of this trait?” (A reminder
for the reader: we are using Williams’ and Lewontin’s notion of an engineering
function, not an etiological function; see Section 1.)
Under both the methodological adaptationist and the evolutionary factors
approach, there are standards of evidence for when a claim for that factor is
supported. When a claim is made that a feature is an adaptation, certain standards
of evidence must be met, such as evidence of fitness contributions or design
features. The same goes for evolutionary by-products/bonuses, or phyletic features;

evidence must be given, in accordance with the standards discussed in Section 1.
Some of the arguments over adaptationism concern these standards of evi-
dence, and nearly all of the focus has been on them, but I claim that some of the
root issues concern the initial research questions.
Which question shall we start with? Is the methodological adaptationist
question really harmless? Or is there something more being imported into the
analysis with that question? Why not use the evolutionary factors research
questions all the time?
3.3 Dangers of Methodological Adaptationism

3.3.1 The “Onerous Burden of Proof” and Its Disappearance
The methodological adaptationists routinely assume that some trait under

consideration is an adaptation. Indeed, the research methods of adaptationism
have proven very fruitful.
The burden of proof has always been on the adaptationists to demonstrate that
a trait has a function and is an adaptation of one sort or another. G. C. Williams
is usually quoted concerning the strong burden of proof required for an adaptive
explanation:
Demonstrating adaptation, Williams argued, carries an onerous burden of

proof. Moreover, “This biological principle [adaptation] should be used only
as a last resort. It should not be used when less onerous principles . . . are
sufficient for a complete explanation” ([Williams 1966] p. 11). Williams did
suggest qualities of trait design that could help build a case for adaptation
(e.g., precision, efficiency, economy) and claimed that formulation of “sets of
objective criteria [of special design]” is a matter of “great importance ([1966]
p. 9). (Andrews et al. 2002a, p. 496; emphasis added).25
But Williams himself applied only an informal probability standard for an

adaptation: “whether a presumed function is served with sufficient precision,
economy, efficiency, etc., to rule out pure chance . . . as an adequate explanation
(p. 10).”26 So Williams himself allowed the “onerous burden” of showing
adaptation to be satisfied, in practice, by something much weaker than the
“objective criteria” he claimed were importantly needed.
Leading behavioral ecologists Hudson Kern Reeve and Paul Sherman (1993)
also assume adaptation under a wide variety of circumstances, rejecting
a widespread definition of adaptation, articulated by the leading philosopher
of biology Elliott Sober, as being too weak. Sober requires, for an adaptation:
25
There is an open question regarding how to read Williams’ strictness on this topic (Lloyd 2013).
26
Andrews et al. 2002a, p. 496; emphasis added.
Adaptation 41
“A is an adaptation for task T in population P if and only if A became prevalent

in P because there was selection for A, where the selective advantage of A was
due to the fact that A helped perform task T.”27
Reeve and Sherman argue there is a big problem with history-laden defin-
itions of adaptation like Sober’s:
Endler’s (1986) survey reveals that . . . knowledge [of selective history] is

available for very few phenotypic attributes. This might mean that the
majority of traits should be considered nonadaptations. Alternatively, it
might suggest the need for a new kind of definition. (Reeve and Sherman
1993, p. 8; emphasis added)
Reeve and Sherman recommend counting more things as adaptations at the

current time, using current utility: “An adaptation is a phenotypic variant that
results in the highest fitness among a specified set of variants in a given
environment” (1993, p. 1). Reeve and Sherman use current fitness to infer
evolutionary history, that is, promoting to “infer evolutionary causation based
on current utility” (1993, p. 2). They claim their approach “decouples adapta-
tions from the evolutionary mechanisms that generate them” (1993, p. 1). This
approach to adaptation is akin to what philosopher Bertrand Russell called the
“method of ‘postulating’,” which he said “had all the advantages of theft over
honest toil” (Russell 1919, p. 71). Thus, an additional problem with methodo-
logical adaptationism in practice is that it is prone to shirking its own “onerous
burden of proof,” that is, the standards of evidence that are set out in Section 1.
It’s easier to change the definition than it is to come up with the evidence of
adaptation, so that is what some adaptationists do!
3.3.2 Mistaking Alternatives as Mutually Exclusive

Rather Than Complementary Accounts
The logic of research questions under the evolutionary factors framework is
a bit different from the logic described by many animal behaviorists, evolu-
tionary psychologists, and other behavioral biology adaptationists, when they
practice their craft of explaining the evolution of interesting organismal
traits.
The evolutionary factors researcher sees the alternative evolutionary factors
as potentially complementary, rather than seeing them as mutually exclusive to
a selective approach. Thus, a given trait can be explained primarily through
a selective force, but also through a genetic or developmental constraint on that
selection, which narrows the range of selective results. In fact, combining
27
Sober in Reeve and Sherman 1993, p. 7.
factors is very common among evolutionary biologists, as in Wright’s combin-

ation drift and selection models (1931), and in the hierarchical selection models
of Wade (1978, 2016) or Odling-Smee and colleagues (2003).
Under the evolutionary factors approach, rather than assuming that a trait is
an adaptation, we can start our examination of any trait by asking: “Does this
trait have a function?”
Also, the evolutionary factors approach acknowledges the division of scien-
tific labor by saying it can be a good idea for some to start by asking about the
function of a trait. Similarly, it would be more useful for a systematist to start by
asking whether a trait is ancestral or “derived,” and more useful for
a developmental biologist to ask how the trait is developed in the organism.28
The question we’re facing in this chapter is: Is it useful for anyone to be
a methodological adaptationist rather than following an evolutionary factors
approach?
For example, contrast the evolutionary factors approach just described with
this dualist methodological recommendation from Andrews et al.:
Because hypotheses about constraint, exaptation, and spandrel, and hypoth-

eses about adaptation are often mutually exclusive to each other, we have
argued that confidence in these alternatives increases only when plausible
adaptationist hypotheses have been considered, subjected to special design
scrutiny, and systematically rejected. (Andrews et al. 2002b, p. 535; emphasis
added in bold; original emphasis in italics)
Andrews and colleagues are making a point here about how to increase confi-
dence in a hypothesis: if A and B are “mutually exclusive” exhaustive compo-
nents, then increasing your confidence in component A commits you to
decreasing your confidence in component B, and vice versa.
But the point is both logically and biologically mistaken, since the evolutionary
components in question are not truly logically mutually exclusive: They can both
be true at the same time. Although being an adaptation and being an exaptation
are not mutually compatible, selection can also occur on a spandrel, making that
combination also compatible.29 Thus, Andrews et al.’s characterizing the factors
as “mutually exclusive” is rarely correct in biology. To assert incompatibility is to
misunderstand the selective and various other evolutionary factors. They are not
only logically compatible, they are biologically compatible.
Mayr (1983) made the same mistake: “Only after all attempts to [find an
adaptive explanation] have failed, is [the evolutionary biologist] justified in
designating the unexplained residue tentatively as a product of chance,” i.e.,
“the incidental by-product of stochastic processes” (Mayr 1983, p. 326; see
28 29
Cf. Beatty 1987. See Table 1.1 for definitions.
Adaptation 43
BOX 3.2 “WHAT EVOLUTIONARY FACTORS ACCOUNT FOR THE FORM AND DISTRIBUTION
“DOES THIS TRAIT HAVE A FUNCTION?”
OF THIS TRAIT,” OR, E.G.,
This question has a series of distinct possible and responsive answers (that
might be considered in any order, except that the adaptive answers usually
go first in practice for the fields under consideration):
A: This trait occurs in the population because it has the function F, an adaptation.
A: This trait occurs in the population, it is under hierarchical selection,
and it has the function G, an adaptation.
A: This trait occurs in the population through mutation and genetic drift.
A: This trait occurs in this population because of mutation and migration of genes
from another population.
A: This trait occurs widely in this population because of an evolutionary develop-
mental novelty.
A: This trait occurs widely in this population because it is genetically linked to
a trait that is highly adaptive (genetic linkage or correlation).
A: This trait has its current form largely because of an ancestral pattern (phyletic
inertia).
A: This trait has its current form and distribution because of pleiotropy with a trait
that was under natural selection.
A: This trait has its current form and distribution because it is a by-product or
bonus of a trait that is strongly selected in the opposite sex in this species.
A: This trait has its current form and distribution because of some combination of
the above factors.
Etc.
Millstein 2008). Similarly, Buss et al. (1998) narrow the alternatives to adapta-
tion down to chance and “incidental byproducts,” omitting all the other alterna-
tives (see Box 3.2). This narrowing creates the appearance of having two
mutually exclusive disjuncts, but in fact, accumulating evidence for one does
not disconfirm all other evolutionary factors.
Modern evolutionary theory says there are evolutionary models available that
use distinct evolutionary causes; any of these may answer the question, “What
evolutionary factors account for the form and distribution of this trait?” Under
this analysis, the causes are not mutually exclusive; they can often be combined
and serve as complementary causes of evolutionary change.
The division of labor response says methodological adaptationists are merely
researchers who look for functional explanations for traits, and if they cannot
find one for a trait, move on to look for another functional solution for another
trait. If that were all they were doing, they would be quite harmless. But that is
not an accurate description of methodological adaptationism in practice. As we
will also see in Section 4, methodological adaptationism leads to bad logic, bad
reasoning about evidence, and inferior biology. It is destructive of good science
and good evolutionary biology; it is not just a matter of overemphasis on
adaptation in the biological community.30
But there are even more serious problems that have arisen from methodo-
logical adaptationism. In practice, methodological adaptationists sometimes
cannot compare the weight of evidence for various hypotheses, one against
the other. Even when consideration of evolutionary hypotheses involving the
other evolutionary factors really does happen, what counts as evidence support-
ing those hypotheses fails to come into view, as we shall see.31
4 Case Studies Showing the Inadequacy of Methodological

Adaptationism
Introduction
We do not usually think that the logic of our scientific methods leads to closed-
mindedness and the inability to see alternatives or evaluate evidence, but that is
exactly what sometimes happens in evolutionary biology of behavioral and
bodily traits with methodological adaptationism, despite its benign reputation.
In this section, we will look at some case studies in which adaptationist
research programs compete with research programs that use other evolutionary
explanations and research questions, focusing on my major case study on the
evolution of the human female orgasm. It is claimed, by both biologists and
philosophers who defend a methodological adaptationist approach, that adapta-
tionist explanations will be abandoned once the evidence makes clear that such an
adaptation approach will not work. I will examine why the research question
“What is the function of this trait?” never seems to fail and never really rolls over
into one of the alternative evolutionary explanations. I analyze why that is so. It is
due to the logic of the research question and its possible and responsive answers.
4.1 The Case of Human Female Orgasm

4.1.1 Bonus/By-product Account of Female Orgasm
I have spent over 35 years researching and analyzing the evolutionary explan-
ations for human female orgasm. In my 2005 book, I analyzed 22 distinct
30
A similar point was made by Wagner in his discussion of shifting pluralism, which is “the idea
that there are multiple causes and mechanisms involved in every evolutionary process” (2000).
31
Suggested Further Reading: Amundson (1994, 1998, and 2005); Carroll (2005); Cosmides and
Tooby (1994); Geary and Flinn (2001); Griesemer (2015); Griffiths (1996); Newman,
S. A. (1988); Newman and Bhat (2008 and 2011); Pinker (1999); Raff (1996) Schmitt and
Pilcher (2004); Symons (1990); Thornhill (1990); Wake (1991 and 2009).
Adaptation 45
theories – all that I could locate at that time – that offered evolutionary explan-
ations for the existence and prevalence of female orgasm; 21 of them were
adaptation accounts. I found that none of these 21 accounts were supported by
the available empirical evidence that we had about female orgasm at that time.
Eleven of these adaptation accounts were based on a pair-bond view of female
orgasm, while several other adaptive accounts were oriented around a female
choice sexual selection view that depended on sperm competition and its con-
comitants (see Section 4.1.4). All of these adaptation accounts were attempting to
account for the persistence of the trait in the human population, not its evolution-
ary origins per se, which might lie in the deep mammalian past, as postulated by
Pavlicev and Wagner (2016). The alternative, nondirectly adaptive account for
persistence is called the “by-product” or indirect selection account, and is based
on strong stabilizing selection in males but not females, as explained below.
The evidential situation has only gotten worse for the 21 adaptive explanations
for the prevalence of female orgasm since my book was published, because in
2013 a study of over 8,000 women was published in which the fitness difference
that orgasm made for women was studied: The genetic component of fitness
difference that the existence and frequency of orgasm made for women was a flat
zero (Zietsch and Santtila 2013). In other words, having orgasm has no effect on
genetic fitness, when measured as number of offspring.32 If things in the past were
like they are today, orgasm cannot have been an adaptation, since it made no
difference to reproductive success, a necessary component for an adaptation. Is
there any reason to think that things were different in relation to female orgasm in
the past? Were pairs in the past more inclined to produce orgasm for the woman
upon intercourse, as many have claimed to me, noting that modern women are
“professional and uptight”? That argument would have to be substantiated with
evidence, which does not look promising according to the world’s authority on
primate sexuality, Alan Dixson (2009, 2012).
I concluded in 2005 that the lone available indirectly selective account (which
relies on substantial stabilizing selection in males), the by-product/bonus account,
had the most evidential support, a position I still hold. The account was first
proposed by anthropologist Donald Symons in 1979. An analysis of Symons’
research shows that he is not a methodological adaptationist in the Mayrian sense,
but rather an “adaptationist” following the path of the evolutionary factors
framework question, “Does this trait have a function?” (See Symons 1990.)
Symons’ account of female orgasm is based on the shared development of the
embryo, as mentioned in the previous chapter. Males and females share the same
32
Ideally, the fitness of female orgasm would be measured by both the quality and number of
offspring, but this was not feasible for the Zietsche and Santtila study. Thus, what we have right
now is a partial picture, but we have no reason to think it misleading.
embryological form at the beginnings of life – they start off with the same basic
body plan, and only if the male embryos receive a jolt of hormones during the
eighth week of pregnancy do any sexually distinguishing characteristics appear.
In males, orgasms are understood to be stabilizing-selected adaptations, likely as
rewards for participation in sexual intercourse, which raises reproductive success.
In fact, while this is always assumed, it is supported only indirectly with evolu-
tionary evidence of the kind we expect from adaptive accounts (Zuk 2006).
The understanding under the bonus/by-product or indirect-selective account of
female orgasm is that the females get the orgasm “for free,” that is, simply as
a consequence of sharing the embryological form with the male, who is under
stabilizing selection for orgasm. The tissues involved in orgasm for males and
females are homologues, shared between males and females, including nerve
tissues, erectile tissues, and muscle fibers. This whole embryological pattern, not
just the clitoris (and potentially involving the five afferent [incoming] sensory
nerve pathways I mention in my 2005 book), is involved in producing orgasm in
females, and is produced in them through their embryological connection to the
same tissues in males. The idea behind the theory is that the tissues involved in
orgasm for males and females are very similar, including nerve tissues, erectile
tissues, and muscle fibers. Thus, females get the functioning orgasmic tissues
through this embryological connection and are capable of having orgasms under
the right conditions of rhythmic stimulation.33 Note that this may be seen as both
an account of evolutionary origins of the trait, as well as a selective account of the
trait’s maintenance in the population.
The bonus, indirect-selective account may also be complementary to the
Ovulatory Initiation Hypothesis of Pavlicev and Wagner, who hypothesize
a deep origin of the female orgasm in the induced ovulation mechanisms,
finding homologies in some of the hormonal releases of both features
(Pavlicev and Wagner 2016, Pavlicev et al. 2019). I find it difficult to understand
what the origins of the male orgasm are supposed to be under this account, but
again, it may well be complementary to the by-product account, and they both
have the same consequences for female orgasm today: Female orgasm is not
adaptive, and it does not have a modern evolutionary function.
In any case, the indirect-selective sort of explanation for female orgasm is both
‘developmental’ and adaptive, as we reviewed in Section 2; female orgasms are
seen as evolutionary “by-products” of adaptive evolution in the males of the
species, just as male nipples are by-products or indirect-selective results of adaptive
evolution in the mammalian females. When I first published my book, this more
33
Komisaruk and colleagues have more recently shown that the human vagina, cervix, and clitoris
are innervated by different afferent (incoming) pathways (2011). More research is necessary.
Adaptation 47
technical use of “by-product” language provoked such a backlash from feminists

who accused me of belittling or dismissing the importance of female orgasm
(despite my having researched and written a book for 22 years about it) that
I have since changed the name to the “bonus/by-product” or more technically
correct “indirect-selective” account, or sometimes, the “fantastic bonus” account.
Let us consider the variety of evidence relevant to this case. Note that we are
considering supporting evidence for the by-product/bonus account. One com-
mon misperception is that supporting evidence for the by-product view must
simultaneously be evidence against an adaptive view of female orgasm; but this
is not this case and rests on seeing the by-product view as a null hypothesis,
which it is not. We will discuss these matters later on in the section.
At the time that my book was published, we didn’t have any fitness results from
women’s orgasm, as we do now, showing the lack of connection between fitness
and orgasm. We did, however, know the distribution of women’s orgasm rates
with intercourse. Since vaginal intercourse is taken to be the behavior most highly
correlated with reproductive success and fertility, orgasm rates with intercourse
were taken to be significant. Figure 4.1 shows the distribution of orgasm rates
with intercourse over a population of women; you’ll notice that the curve is
relatively flat, compared to the curves in the selective models shown in Figure 1.3.
This comparably ‘flat curve’ is represented by an x-axis of overall orgasmic
performance, while the y-axis represents frequency in the population.34 It shows
that the orgasm rate with intercourse never rises above 20 percent for any
segment of the female population, in contrast to the selection curves that you
see in Figure 1.3 (in Section 1), where the curves feature large percentages of
the population – along the lines of 70–90 percent – on the desired value of the
trait. Only about 13 percent of women always have orgasm from intercourse
(and about half of that is from “assisted” orgasm, that is, orgasm assisted by
hand or vibrator stimulation during intercourse), and roughly a third of women
rarely or never have orgasm with intercourse, while 5–10 percent of women
never have an orgasm at all from any means. The rest fall between – sometimes
do, sometimes don’t have orgasm with intercourse. But, again, as we noted in
Section 1 and saw illustrated in Figure 1.3, simple directional or balancing
selection, which is supposed in nearly all of the selection stories of female
orgasm, usually produces substantial peaks in the distribution curves of a trait,
peaks encompassing 70–90+ percent of the population. (There is an exception
to this expectation; see Section 4.1.4). The fact that women vary so widely in
their orgasmic performance thus provides very suggestive evidence that nearly
34
This curve was drawn from statistics from Dawood and colleagues 2005, but it conforms well
with my analysis of typical numbers from the 35 studies that I reviewed in my 2005 book, which
covered 66 years of research involving over 141,200 women.
Population frequency on y-axis

100%
90%
80%
70%
60%
50%
40%
30%
20%
10%
0%
0 100
Orgasm with intercourse (percent) on the x-axis
Figure 4.1 Orgasm rates with intercourse taken from Dawood and colleagues
2005
all of the selection explanations offered so far for female orgasm – no matter
what their details are – are likely unsupported or disconfirmed. The most recent
selective accounts published since my book (for example, Puts and colleagues,
2012a,b) do not address this issue of the lack of a selective peak.
Consider a further variety of evidence for the by-product/bonus account.
Strikingly, females masturbate through direct stimulation of the clitoris – the
homologous organ to the penis, from the same sources in the embryo – and not
through simulating intercourse, just as we would expect on the by-product
account. Similar stimulation to homologous organs yields orgasm for both
sexes (Kinsey and colleagues 1953). Note the contrast with what we would
expect about masturbation if orgasm were selected to go along with intercourse,
as it does on all of the adaptive theories: Women would imitate reproductive sex
when they masturbated.
In fact, only 1.5 percent of women do this, according to Hite (1976) and
confirmed by Kinsey et al. (1953). Thus, the fact that women stimulate the
homologous organ to the penis when they masturbate is predicted by the by-
product/bonus account. The origins and maintenance of female orgasm lie with the
male-homologous orgasmic structures and reflex (i.e., the clitoris and surrounding
tissues), and not in relation to intercourse. The fact that this prediction of the by-
product/indirect-selective account is confirmed is evidence in favor of the account.
These facts about masturbation are precisely why Freud thought it necessary
to move the locus of excitement from the clitoris to the vagina for “mature”
women, because it didn’t make evolutionary or adaptive “sense.” Freud
Adaptation 49
believed that all women ought to have orgasm from vaginal intercourse. This
belief was explicitly derived from his conviction that female orgasm must be an
evolutionary adaptation to promote reproduction, like many present-day
explanations of the trait.
Freudianism said: Female erotic pleasure is initially centered on the clitoris in
infancy and childhood, but with the process of maturation into womanhood, the
core of female eroticism must ‘migrate’ to the vagina as the healthy woman’s
‘primary’ erotic center (Freud 1905).
As Freud wrote:
In her childhood, moreover, a girl’s clitoris takes on the role of a penis

entirely: it is characterized by special excitability and is the area in which
auto-erotic satisfaction is obtained. The process of a girl’s becoming a woman
depends very much on the clitoris passing on this sensitivity to the vaginal
orifice in good time and completely. In cases of what is known as sexual
anaesthesia in women the clitoris has obstinately retained its sensitivity.
(Freud [1923] 1963, p. 318).
Women who failed to enact this migration – that is, the 90–94 percent of women
who “obstinately” remained dependent on the clitoris for orgasm, or who failed
to reliably have orgasm from intercourse without additional clitoral stimula-
tion – were ‘infantile,’ ‘immature,’ ‘neurotic,’ ‘frigid,’ or ‘dysfunctional.’ Each
of the labels is an assault on women’s well-being itself. It’s very significant that
this labeling was not restricted to some medicalized or head-shrunken subset of
the population – it was the coin of the realm, in women’s magazines and advice
columns, in doctors’ advice, and in marriage manuals.
But rather than follow the other evolutionary explanations in enforcing this
abuse, the bonus/by-product indirect-selective account actually explains the
low rate of reliable female orgasms with intercourse.
It is also supported by new anatomical studies linking the structure of the
genitals with orgasm rate with vaginal intercourse. Behavioral endocrinologist
Kim Wallen and I discovered that women with a longer distance between their
clitoris and urinary meatus (urinary opening, as a more stable substitute for
a measure of vaginal opening, the CUMD, “Clitoral-Urinary-Meatus-
Distance”) have many fewer orgasms with intercourse than those women with
a shorter distance.35 Note again that the occurrence of orgasm is not correlated
with fitness measures, so these different distances cannot be interpreted func-
tionally, under the present information. The correlation we discovered seems to
be an accident of development, not a product of genes, which is confirmed
35
Wallen and Lloyd 2011; independently confirmed through MRI by Oakley et al. 2014; Vaccaro
2015.
independently by animal studies (Wallen and Lloyd 2011; see discussion and
Figure 4.2 in Section 4.1.4).
Symons’s general thesis is also supported by the nonhuman primate evi-
dence. For example, female stumptail macaques have been shown to have
orgasms by placing electrodes into their uteruses and genitals – which shows
that they have the distinctive contractions and other bodily markers character-
istic of orgasm.
There is a fascinating thing about these orgasms, though. Many of them occur
when one female climbs onto the back of another female and rubs her clitoris
against the other one’s back, thus providing the direct, rhythmic stimulation
desired for orgasm. A few of these same females also have orgasms while
copulating with males, but these rates tend to be quite low (Lloyd 2005a). In
addition, none of the observations about homosexual orgasms were observed to
occur during the monkeys’ fertile periods, thus denying any account based on
hormones.
All of this is bad news for evolutionary theorists attempting to tell adaptive
stories of female orgasm that tie it to heterosexual copulation or fertility, with
which this evidence is incompatible. For example, the adaptive hormone-based
account of female sexuality says that orgasm will occur during the estrus period
of the animal (i.e., when it is fertile), but this is not what is found here, where the
orgasms all occurred outside the fertile period, and cannot therefore be related
to fertility. These orgasms, however, that are unrelated to heterosexual copula-
tion and to fertility are completely compatible with Symons’ by-product/bonus
account, as they link the clitoral stimulation to penile stimulation of the male.
This behavior is not compatible with any of the proffered adaptive accounts of
female sexuality (Lloyd 1993).
4.1.2 Adaptationist Responses to the Bonus/By-product Account

of Female Orgasm
In a 1987 discussion in Natural History of my early work presented by Stephen

Jay Gould, on the evolution of female orgasm, Gould discussed a variety of
empirical evidence in favor of Symons’s by-product/bonus view. Adaptationist
Donald Dewsbury, a distinguished psychologist studying animal reproductive
behavior, claimed in response to Gould’s discussion
But Gould (1987a) goes too far in asserting that “female orgasm is not an
adaptation at all” (p. 17). We need to study the consequences of [female]
orgasm for differential reproductive success and then determine whether
a plausible case can be made for drawing the loop from present consequences
to the past history of natural selection. These need to be studied, not asserted
or denied a priori. (Dewsbury 1992, p. 103; my emphasis)
Adaptation 51
But Gould is actually representing Symons’ views in his quote, and Symons’
views are based on empirical data presented in his chapter; they are not asserted
a priori. Gould’s full quote says: “In all the recent Darwinian literature, I believe
that Donald Symons is the only scientist who presented what I consider the
proper answer – that female orgasm is not an adaptation at all. (See his book,
The Evolution of Human Sexuality (1979)).” (Gould 1987a, p. 17).
Gould also says:
Elisabeth Lloyd, a philosopher of science at the University of California at

San Diego, has just completed a critical study of explanations recently
proposed by evolutionary biologists for the origins and significance of female
orgasm. Nearly all these proposals follow the lamentable tradition of specu-
lative storytelling in the a priori adaptationist mode. (1987a, p. 17)
But Dewsbury’s perception was, clearly, that no good evidence had entered into
the debate, despite Symons’s entire book chapter detailing empirical evidence
supporting his theory, and Gould’s appeals to the empirical support that I had
amassed, involving 14 studies at that time. But all of that empirical evidence
(discussed in Section 4.1.3, “‘Null’ Hypotheses”) was invisible to these
researchers. Apparently adaptive hypotheses could be favored or disfavored
by the evidence – and they had not been favored in the female orgasm case so
far – but a nonadaptive hypothesis like the by-product/bonus account apparently
could only be “asserted or denied a priori.”
Similarly, many years later, evolutionary psychologists Andrews and col-
leagues, in considering Gould’s discussion of the female orgasm, claimed that
Gould gave no positive evidence for the trait not being an adaptation, under either
the contemporary fitness view of adaptation or under a historical functional
account, and simply “proclaimed that the female orgasm is not an adaption but
a byproduct.”36 Andrews et al. complain about Gould’s methodology that:
Gould’s conclusion may be correct but his argument does not warrant it. As
we point out later, demonstrating that the female clitoris and orgasm are
byproducts requires the failure to find evidence for its special design and,
hence, an adaptationist testing strategy. (Andrews 2002a, p. 499)
Note Andrews and colleagues’ requirements of the evidence for something to

be shown to be a by-product/bonus. They complain that Gould did not fulfill
their evidential requirements, which did not concern positive evidence for
the by-product account, but rather, failure at finding an adaptation.37
36
See Box 4.5 to see the rankings of the strength of evidence and sources for these features of the
evidence for the indirect-selective by-product account.
37
This is a summary of supporting evidence, not a summary of evidence against an adaptive
account (see Section 4.1.3).
BOX 4.1 VARIETY OF EVIDENCE SUPPORTING THE BY-PRODUCT ACCOUNT38

Developmental homology between penis and clitoris,39
Developmental homologies between male and female nerve fibers and

pathways, and erectile tissues
Female masturbation techniques focused on the clitoris, not reproductive

sex (intercourse)
Low rates of female orgasm with reproductive sex

Female orgasm in nonhuman primates (outside of intercourse and estrus)
Correlation of unselected female anatomical traits with orgasm with
intercourse40
But actually, the repeated failure of adaptationist accounts does not have any
bearing on the positive evidence available supporting the bonus/by-product
account (reviewed in Box 4.1), although many adaptationists incorrectly
believe that this failure of the adaptationist accounts is the sole evidence
supporting that indirect selective explanation.41
As we’ll see later on, because the logic of the methodological adaptationists’
research question demands exclusively a function answer, no bonus/by-product
answer can be considered a positive answer to their research question, and thus
bears support in its favor.
But what about the other evolutionary factors that are allowed in all
evolutionary textbooks? Reeve and Sherman (1993) allow that there are
“mechanisms of persistence other than natural selection,” and they list them
as follows: “a relatively non-adaptive trait may persist because of several
processes including prolonged lack of genetic variation, unbreakable genetic
correlations with other traits, recurrent immigration, and genetic drift” (Reeve
and Sherman 1993, p. 19). But it turns out that in practice they take these
alternative causes, such as developmental constraints or genetic correlation, to
either actually be serving the adaptive functions as well, or to not really be
viable as alternative causal explanations to adaptive explanations. From this
we can see why the list of answers to the methodological adaptationist
research question does not actually include any other answers besides the
function ones.
38
See Section 4.1.4. 39 Andrews et al. 2002a, p. 499 footnote 6: p. 504.
40
Alcock 1987, 1998; Sherman 1989; see Lloyd 2005a for discussion.
41
See Alcock 1998; Linquist 2006; Mayr 1983, p. 326.
Adaptation 53
4.1.3 “Null” Hypotheses

Ritual recitation of Gould and Lewontin’s “Spandrels” paper in the adapta-
tionist literature usually includes only the lesson that not everything is an
adaptation. But this misses one of the primary points of their paper, which
includes the problem of the neglect of developmental constraints, phyletic
inertia, and laws of form as evolutionary causes. Attention to the logic of
research questions illuminates this problem. How can these other factors
ever appear on the methodological adaptationist’s list of real, responsive
answers?
I argue that methodological adaptationists are committed to this neglect by
the logic of their initial orienting question. Once this first move of committing to
the question “What is the function of this trait?” is carried out, which seems so
innocent, methodological adaptationism is rationally going to lead to error in
some cases. This is because starting our biological inquiry by asking the
methodological adaptationists’ function-question involves treating nonadaptive
hypotheses as something like statistical nulls.
For example, David Barash says explicitly, in a discussion regarding the by-
product/bonus theory of female orgasm, that the possibilities include “the ‘null
hypothesis’ that it might not be a direct product of evolution after all” (2009,
p. 133).42
In general usage in science or biology, a “null hypothesis” is usually
a negative alternative to a positive correlational hypothesis, often used in
Neyman-Pearson statistical analyses, one that binds together two variables or
terms in a pattern of relations. The use of the “null” hypothesis by behavioral
biologists tends to be much more informal, and not to signify necessarily the
application of any formal statistical test at all. The positive hypothesis in this
case would be one in which a genetic or phenotypic trait was positively
correlated with fitness or some component of fitness, while the null hypothesis
would be simply a noncorrelation with fitness, often indicating nonselection. An
example will bring this out.
John Alcock is the author of the leading textbook on the evolution of
animal behavior, but he writes about Gould, who is following my non-
adaptive approach to female orgasm: “These are not the claims of someone
who wishes to expand the horizon of evolutionary analyses but instead are
designed to marginalize the adaptationist approach.” Alcock is thus equat-
ing evolutionary causal analyses with adaptationist analyses exclusively
(1998, p. 332). This neglects the fact that the by-product account of female
42
By “evolution,” Barash means “selection,” in context. This mistake is discussed in the next
section.
orgasm by Symons is, in fact, an evolutionary causal analysis in its own

right.
In another paper, Sherman simply assumes what needs to be shown:
Alcock (1987) had good reasons to question how a structure that plays such
an intricate role [in facilitating sexual pleasure in women—here, he is talking
about the clitoris, not the orgasm, inappropriately] and one so obviously
related to fitness could possibly be reproductively neutral. (1989, p. 698,
emphasis added)
The adaptationists continue to behave as if there’s no supporting evidence for

the by-product view, seeing the view as being essentially negative: They see the
by-product view as claiming only that no adaptive account has been found,
rather than as a positive causal story of indirect selection and its by-products in
its own right. Hence their attitude that adopting the by-product view as a live
alternative to an adaptationist account of the trait is tantamount to “giving up”
on an evolutionary account altogether.43
This, however, is the wrong standard scientifically. It presents the scientific
situation as all-or-nothing, the adaptation account or no scientific account at all.
The by-product/bonus theory is a causal evolutionary account and has its own
kind of evidence in its favor (see Beatty 1987 for a parallel point about genetic
drift). Analysis of the logic of research questions helps make the source and
nature of this confusion quite clear.
Let’s review the questions asked by the methodological adaptationists and the
researchers using the evolutionary factors framework and their samples of
relevant well-formed answers here.
As can be seen by analysis of the logic of these research questions in Box
4.2, then, those using the methodological adaptationist approach cannot
appreciate the accumulated positive evidence (see Box 4.1) for the by-
product/bonus approach, because they take it as equivalent to a null
hypothesis. The by-product account involves positive stabilizing selection
on the males, and embryological evidence supporting the linking of the
relevant trait with the females of the selected trait, among other evidence,
as listed in Box 4.1. This evidence is in some sense only visible on the
evolutionary factors framework, where the weight of evidence is the right
approach to use in evaluating the by-product/bonus causal hypothesis and its
alternatives.
43
For example, see the language in Alcock 1987, 1998; Sherman 1989.“The adaptationist position
is an invitation to scientific investigation,” writes Alcock, and this is meant to contrast with the
by-product account, which, it is implied, stifles inquiry prematurely, resting with an unsatisfac-
tory, incomplete explanation (1987, p. 6; Lloyd 2005a p. 156 and Ch. 6).
Adaptation 55
BOX 4.2 ANALYSIS ACCORDING TO THE LOGIC OF RESEARCH QUESTIONS

Methodological Adaptationists: “What is the function of this trait?”
A: The function of this trait is F.

A: The function of this trait is H, or I, J . . . Z, AA. . . ?
Faulty, Nonresponsive Answer: This trait has no known function or
correlation with fitness, and may not be a direct product of selection at
all (i.e., adaptationists’ “null” hypothesis, which Barash treats as equiva-
lent to the bonus/by-product hypothesis)
Evolutionary Factors Approach: What evolutionary factors account

for the form and distribution of this trait? Does this trait have a function?
Possible and Responsive Answers, often used in combination:
A: This trait occurs in the population because it has the function F, an

adaptation.
A: This trait has its current form and distribution among one sex largely because it
is a by-product or indirect product of stabilizing selection and genetic linkage on
the opposite sex’s trait. (The methodological adaptationists’ mistaken “null
hypothesis” actually is an independent causal hypothesis, which can have its
own positive evidence.)
A: This trait occurs widely in this population because it is genetically linked to
a trait that is highly adaptive.
A: This trait has its current form largely because of an ancestral developmental
pattern that provides a contemporary developmental constraint.
A: This trait has its current form and distribution largely because of a phyletic
pattern from an ancestor that is continued in this trait.
A: Combinations of above factors
A: etc.
Two points emerge from the discussion above.

First, characterizing the by-product/bonus alternative as a “null” hypothesis
leads to the impossibility of positive evidence for what is, in truth, a causal
hypothesis, which needs empirical support or refutation. Thus, the attribution of
a “null” is mistaken.
Secondly, both the methodological adaptationist and the evolutionary factors
theorist can ask about adaptive traits or functions, but the full meaning of the
question will not be revealed until we can see what list of answers are live
options and under full consideration. As we have seen, the methodological
adaptationists may claim to have the same items on their lists as the evolution-
ary factors theorists, but when push comes to shove, they do not treat them as
live options, on their own accounts.
We can zero in on the key problem: None of this evidence for the causal by-
product/bonus hypothesis in Box 4.1 is recognized or weighed when consider-
ing this trait from the adaptationist methodological perspective. Thus, even
though the methodological adaptationists present their adherence to their
research program and its attendant question as perfectly harmless and, in fact,
very good and productive science, we can see here an example of where it goes
astray. Because they implicitly assume that no null hypothesis may have
evidence in its support, they cannot see the evidence supporting the by-
product/bonus account.
4.1.4 Critics of the By-product Account and Evidence
The leading critics of the by-product/indirect selection account continue to

support adaptive accounts. Let us compare the status of the empirical evidence
supporting the most favored current adaptive account (Puts et al. 2012a,b,
Box 4.4) with the evidence supporting the bonus/by-product account, as given
in Box 4.1. Recall that, according to 37 studies of 148,346 women using 27
metrics in the various studies, only about 20 percent of women reliably have
orgasm with intercourse, including with hand-or-vibrator-assisted intercourse,
while about 90 percent of the female population does have orgasm sometime
during their lives (Lloyd 2005a). So, while orgasm is present in the vast majority
of women, it does not routinely appear in the ordinary evolutionarily relevant
context, that is, vaginal intercourse.
The by-product/bonus account gives a cogent explanation for this glaring
fact. However, we should note that not every evolutionary explanation must
produce frequent orgasm with intercourse, under our current theories. Consider
a female choice account with sperm “upsuck,” as shown in Box 4.3.
Puts and colleagues’ female choice/upsuck account posits that females mate
multiple times over a short period of time with different males. The basic idea is
that the female will have orgasm preferentially with the higher-quality males.
Orgasm is assumed to be accompanied by a mechanism of uterine upsuck that
makes it more likely that the female will be fertilized by the higher-quality male.
Thus, the orgasmic women are required to respond with orgasms only some-
times with intercourse – “yes” with high-quality males, and “no” with lower-
quality males. The model says this will produce more and/or better offspring. In
Box 4.3 there is the sketch of the female choice selection model and its level of
evidence. But look at their data (Box 4.4).
Adaptation 57
BOX 4.3 FEMALE CHOICE/UPSUCK MODEL OF FEMALE ORGASM AND ITS EMPIRICAL
EVIDENCE
Trait – [Mate with multiple males]: Fair evidence44

Trait – [Female orgasm preferentially with high-quality males]: Fair evidence45
Trait – [Uterine upsuck]: Evidence against46
Hereditary basis – [Orgasm’s heritability]: Good evidence47
Connection to fitness – [More and better offspring with higher orgasm frequency]:
Evidence against48
Selection pressure – [Strong pressure on women to have offspring of high-
quality fathers; female choice, sperm transport]: Poor evidence49
Alan Dixson, again, the world authority on comparative primate sexuality,

denies that this sort of “cryptic female choice” selection occurs in human beings
(2012, p. 630), in which females have a mechanism to “choose” or prefer the
sperm of higher-quality males to fertilize their eggs. Dixson gives a series of
reasons why this is not so, including the lack of specialization in the penis, the lack
of specific structures in the sperm, the lack of evidence for uterine upsuck,50 and so
on, all of which, in other species of primates, accompany cryptic female choice and
sperm competition as hypothesized in the upsuck theory, and its associated
hypothesis of female choice.
Under the upsuck theory, female orgasm is accompanied by a sucking motion
of the uterus. This “uterine or sperm upsuck” theory is an old piece of folk
wisdom dating back to the Ancient Greeks, but it has never enjoyed any real
evidential support, although people have been seeking scientific evidence to
support it for over 70 years. There is actually evidence against it from a set of
nicely designed experiments done by Masters and Johnson in the 1960s (1965;
1966)
Nevertheless, the upsuck hypothesis is very widely believed by laypeople,
especially due to a deceptive narration of a video clip shown on TV,51 and had
achieved widespread acceptance among scientists since the 1990s, through the
work of Robin Baker and Mark Bellis published in 1993, which claimed to
provide empirical evidence supporting the phenomenon.
44
Puts et al. 2012a,b. 45 Puts et al. 2012a,b, giving them the benefit of the doubt.
46
Levin 2011; Masters and Johnson 1965, 1966; Dixson 2009; 2012.
47
Dawood et al. 2005; Dunn et al. 2005. 48 Zietsche and Santtila 2013.
49
Puts et al. 2012a,b. See Lloyd 2005a, Ch. 7; Levin 2011, 2015; Dixson 2012 for critiques.
50
See Levin 2011 for further evidence against sperm upsuck.
51
While the video only showed the contractions of the uterus upon orgasm dipping down into the
vaginal cavity, where the sperm lay, the narrator added that “upsucking” of the sperm was also
happening, although we cannot witness that.
BOX 4.4 VISUALIZATION OF BAKER AND BELLIS 1993 DATA SET FROM PAIRS IN STUDY
Baker and Bellis (1993)

Count of Observations by Pair
(Total = 127)
Pair
A 9
B 93
G 1
H 1
N 2
Q 1
R 8
S 6
W 3
Z 2
AA 1
0 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100
Observations
In one “supporting” data set, they have 1 out of 11 couples in the sample
contributing 93 out of the 127 data points (nearly three-quarters of the data!). Four
of the other 10 couples contributed one data point each, a combined total of
3 percent of the data, and so on. But extrapolating to the population at large based
primarily on the results of a single subject badly violates standard statistical
practice (see Lloyd 2005a, Ch. 7). In the end, the Baker and Bellis data are
statistically worthless and no scientific conclusions can be drawn from them.
So why was this account of uterine upsuck adopted by top researchers in
human evolution and taught in human evolution courses by evolutionary psych-
ologists and sociobiologists? It cannot be because the paper was good science –
because it clearly wasn’t – as even my harshest critics now agree (e.g., Barash
2005). It seems to be because they just liked what the paper had to say, namely
that female orgasm serves an evolutionary function. Here we see adaptationist
bias in action, and several adaptationists, David Puts and Khytam Dawood and
colleagues, are still citing this Baker and Bellis paper to underpin their female
choice theories (e.g., Puts et al. 2012a, b) despite having given no real defense of
the paper against the critique I gave in 2005, among other methodological
critiques.
Adaptation 59
In Box 4.3 is the state of the empirical evidence supporting the various
aspects of the female choice/upsuck selection model, accompanied by their
sources. As you can see from Box 4.3, the model is not well supported by the
empirical evidence.
But if we look just at the prediction of this particular sexual selection model,
it can successfully be tweaked to fit the evidence of the flat curve showing
orgasm rate with intercourse, as in Box 4.1. The poor state of evidential support
for the hypothesis is only made clear by checking the independent evidence for
the various aspects of the model, the central and crucial step in evaluating an
adaptive hypothesis, as we saw in Section 1. Thus, the only adaptive model that
is compatible with the sexology evidence – in that it fits the flat curve – does not
have further supporting evidence for its aspects and assumptions. Thus, the
female choice model is not comparable to the by-product account in its overall
evidential support.
There is further evidence in favor of the by-product account. One of the
most compelling things about the female choice theory is that it gives an
answer to the question “Why do women respond to intercourse with orgasm
sometimes yes, sometimes no?”, which was mysterious under other adaptive
theories.
Kim Wallen and I published independently confirmed analyses of data that
bear directly on whether or not women have orgasm with intercourse, and
when. As mentioned above, our anatomical, non-adaptive, explanation of why
women have a variety of orgasm rates is based on what we call “CUMD”
measurements, the measured distance between the clitoris and the urinary
opening, meant to stand in as a proxy for the vaginal opening.
Figure 4.2 shows some of our data.
3.5 Orgasm
No Orgasm
3.0
CUMD (cm±SEM)
2.5
2.0
1.5
1.0
0.5
0.0
Bonaparte Landis Combined Autosexual
(Masturbation)
Study Sample
Figure 4.2 Wallen and Lloyd CUMD

The white bars represent women who reliably do have orgasm with inter-
course, while the black bars represent women who routinely do not have orgasm
with intercourse. On the y-axis is the CUMD.
You can see that the women who routinely have orgasm with intercourse have
much shorter CUMD measures than the women who do not. The difference
between the groups in orgasm rate is highly significant, greater than two standard
deviations, in both data groups that we analyzed, Bonapart and Landis. This
anatomical trait is apparently due to developmental exposure to androgens in the
womb and is not genetically controlled.
Using an independent statistical test, we also found that this anatomical
distance was predictive of whether a woman had orgasm with intercourse. You
can also see that it was irrelevant to orgasm with masturbation, as we would
expect.
In other words, we found that an anatomical trait predicted whether or not
a woman would have orgasm with intercourse. This makes good sense, if you
think about it. In sum, Wallen and I found that for the strong majority of women
in our samples, anatomy seems to suggest destiny (2011). And clearly, if her
anatomy so strongly influences whether or not she has an orgasm with inter-
course with a male, that leaves insufficient room for the genetic quality of the
male – specifically, his masculinity, attractiveness, or dominance, as presented
in the female choice theories – to strongly influence the outcome of such
intercourse, with orgasm accompanied by uterine upsuck.
This is because, according to the population genetic theorists, the selection
pressure of this type of sexual selection scenario needs to be quite strong in
order to produce any result in terms of evolution (Hosken 2008). Thus, the
anatomical relation we discovered makes such a scenario highly unfeasible. In
other words, there is no evidence that the women’s variation in orgasmic
response, as measured in CUMD, coordinates with the masculine features
emphasized by the female choice theories. It seems, rather, that women either
tend to have orgasm with intercourse or not, depending upon their anatomical
features and not their partners. As we move along the flat curve, those women
either tend or don’t tend to have orgasm with intercourse, regardless of their
male partners. But the prevailing selective theory needs them to be very sensi-
tive to male traits against the available evidence.
Thus, the female choice theory does not have further supporting evidence for
its aspects and assumptions, and thus is not comparable to the by-product
account in its overall evidential support, as one can see by following up on
the evidence cited in the footnotes. We can see this quite clearly when we
contrast this sexual selection/cryptic female choice adaptation model (Box 4.3)
with the one for the bonus/by-product/indirect selective account (Box 4.5).
Adaptation 61
BOX 4.5 EMPIRICAL EVIDENCE FOR THE BY-PRODUCT/BONUS HYPOTHESIS
Trait – [Developmental homologies between orgasmic tissues]: Excellent

evidence
Trait – [Effectiveness of female masturbation in producing orgasm]: Excellent
evidence52
Trait – [Low rates of female orgasm with intercourse]: Excellent evidence53
Trait – [Female orgasm in nonhuman primates]: Good evidence54
Hereditary basis – [Orgasm’s heritability]: Good evidence55
Connection to fitness – [NO correlation with fitness]: Good evidence56
Note that in both cases, there is evidence for no function of orgasm in

females, which is nonresponsive to the research question of the methodological
adaptationists, “What is the function of this trait?” Instead, the by-product
/bonus explanation is better seen as an answer to the evolutionary factors
research question, “What evolutionary factors account for the form and distri-
bution of this trait?”
This is the correct reading of the bonus/by-product theory of female orgasm,
as a positive alternative causal hypothesis, not as a null hypothesis. It is an
alternative to the previous, function answers to the methodological adaptation-
ists’ question, and it is an answer that is not on their list of possible answers,
which only includes answers like: “The function of female orgasm is to prefer-
entially mate with high-quality males,” or “The function of female orgasm is to
aid the pair bond,” and so on.
To illustrate the dangerous and unscientific consequences of methodological
adaptationism in this particular case: Several prominent adaptationists repeat-
edly complain that under the by-product/indirect selection hypothesis, female
orgasm would fade away and deteriorate over evolutionary time and would
disappear from the population. This mistaken inference has been advanced not
only by leading scientists such as Alcock, Sherman, and Barash, but also by
feminist primatologist and human evolutionist Sarah Blaffer Hrdy, and it is
based on a misunderstanding of both how the by-product/bonus account works,
and the evolutionary factors framework itself.57 These misunderstandings are
52
Kinsey et al. 1953; Hite 1976; Fisher 1973.
53
Kinsey et al. 1953; See summary of 47 studies, 140,000+ women in Lloyd 2005a.
54
See summary in Lloyd 2005a; Lemmon and Allen 1978; Chevalier-Skolnikoff 1974.
55
Dawood et al. 2005; Dunn et al. 2005.
56
Dawood et al. 2005; Dunn et al. 2005; Kinsey et al. 1953; Komisaruk et al. 2006; Lloyd 2005a;
Zietsch and Santtila 2013.
57
Alcock 1998; Sherman 1989; Smith (Hrdy) 2005.
likely a consequence of their adaptationist bias that a particular trait will only be
sustained in a population if it itself is under sustained selective pressure. But
under the bonus/by-product account, the basic muscle, nerve, and tissue path-
ways involved in female orgasm would be maintained in the female over the
generations in virtue of the fact that they are under ongoing strong stabilizing
selection in the male; male nipples are maintained in the same fashion. Nobody
thinks that male nipples are disappearing! Thus, methodological adaptationist
explanatory biases involving the necessity of selection have led to fundamental
mistakes regarding the by-product/bonus hypothesis by these researchers and
their followers.
In addition, when discussing alternatives to adaptations, methodological
adaptationists have been prone to make further scientific errors concerning
what the by-product/bonus account says and assumes. These biologists rea-
son that if a trait is not adaptive, it cannot be part of an evolutionary account
at all.
On John Alcock’s analysis, the by-product/bonus hypothesis is a null result and
offers only a “proximate” explanation of how women come to have orgasms.
For Alcock, who calls himself an “ardent adaptationist,” the by-product
explanation is seen as no evolutionary explanation at all. On Alcock’s analysis,
which is shared by Paul Sherman, a leading theoretician of animal behavior, the
by-product hypothesis offers only a “proximate” explanation of how women
come to have orgasms. In other words, it only explains how female babies grow
up to have orgasms as adult women.
Alcock writes that
proximate explanations of a biological characteristic do not make it impos-

sible to ask whether the trait of interest contributed to individual reproductive
success in the past or does so currently . . . If we were to discover the female
orgasm occurred with positive effects on female reproductive success, we
would gain an evolutionary dimension to our understanding of this trait that is
not covered by any proximate explanation. (emphasis mine, emphasis his,
Alcock 1998, p. 330)
Thus, the by-product account is not seen as an evolutionary account at all – it is

not an answer to any evolutionary question about female orgasm, with support-
ing evidence and theoretical standing in evolutionary theory.
Here we can also look to David Barash, the author of the most widely selling
textbook on sociobiology for a couple of decades and a grandfather of the field
of human evolution, who writes, with his wife, in a sympathetic discussion
regarding the impetus behind those favoring the by-product/bonus theory, that it
involves
Adaptation 63
a scientifically legitimate desire to explore all possible explanations for any

biological enigma of this sort, including the “null hypothesis” that it might
not be a direct product of evolution after all. (2009, p. 133; my emphasis)
Note the equivalence of evolution with selection in this statement; the bonus/by-
product explanation is mistakenly not considered evolutionary, just as we saw
before with Alcock and Sherman. This is again the result of the logic of the
research question, through methodological adaptationism.
For these authors, unless we are allowed to assume there is an adaptation,
then we cannot tell whether we can explain it in an “evolutionary” way. The
entire rest of evolutionary biology that we have been discussing in the evolu-
tionary factors methodology is invisible, under this account; it is disappeared.
The methodological adaptationists’ methodology was supposed to be benign; it
was not supposed to be a risky endeavor with radical theoretical commitments,
although that is where it seems to have ended up.
4.1.5 Beyond the Comfortable Boundaries of Adaptation: The Logic

of Research Questions
In this section, I have been emphasizing the initial patterns of inference and
explanation, of exploration and investigation, rather than the final “evidentiary
standards,” that are often emphasized and discussed when considering adapta-
tions. My focus here is much more on the investigative standards, and less on
the evidential standards. My point is that if you use the methodological adapta-
tionist research question, the evidentiary standards of alternatives like the by-
product/bonus view, accurately portrayed, never come up, since they are buried
under the assumptions regarding the null hypothesis and other myths. Gould
and Lewontin’s just-so story objection is about the standards of evidence, but
I have identified the deeper danger earlier, which is in the logic of the research
questions asked, particularly in the consequences of the methodological adap-
tationist research question and its possible and responsive answers all being
“function” answers.
Many adaptationist researchers approaching the evolution of female orgasm
start with the methodological adaptationist research question:
“What is the evolutionary function of female orgasm?”
Other evolutionists, though, may ask:
“What evolutionary factors account for the form and distribution of
female orgasm?”
My claim is that the possible and responsive answers to these evolutionary
questions are relevantly and significantly different. These are questions and
answers with consequences.
For instance, an evolutionary account of female orgasm is used to underpin

a notion of the normal function of female orgasm for the diagnostic and
statistical manual of the psychiatric profession, the DSM V by which sexual
disorders are diagnosed.58 But in evolutionary science, there is no single
accepted adaptive account of female orgasm, and thus no notion of its ‘normal
function,’ if it has any at all.
The fact that the adaptationists see the by-product view only as a null
hypothesis or as a nonanswer to the adaptive question leads directly to their
mistaken characterizations and inferences involving the view. I am concerned
with what it would take to get a community of adaptationists to move far enough
beyond their research orientation and their driving adaptationist question to start
approaching things from the broader, evolutionary factors point of view.
What would it take for these researchers to consider seriously the alternatives
of the evolutionary factors approach, which are acknowledged to be real
contenders for valid evolutionary explanation?
This case of the female orgasm reveals that there is something peculiar and
implausible about methodological adaptationism as it’s usually advanced,
namely, that the researcher is envisioned as, at some time in the middle of
their research program, abandoning their research commitments and explana-
tory practices, in the face of some facts or others, and then going along some
completely different explanatory pathway. This is a lot to ask a researcher to do;
they need to do a sort of mental gymnastics, and few – in fact, none – of the
methodological adaptationist researchers involved with the evolution of female
orgasm have been able or willing to do that.
In sum, this case highlights issues with the evidence needed for adaptive
explanations that are pertinent to the study of development and by-products, and
how confusing to biologists it sometimes is to move beyond the comfortable
boundaries of assuming that a trait is an adaptation.
Let us consider some other cases in which developmental biology and
developmental genetics play a significant role in evolutionary explanation and
examine how adaptation explanations might work in counterpoint to evolution-
ary factors ones.
4.2 Development and the Case of the Salamander Toes

Recall from Section 2 the four-toed salamanders. This interesting case of com-
peting explanations between adaptation and other evolutionary factors research
58
The presence of a “marked delay in, marked infrequency of, or absence of orgasm” is used in the
definition of a sexual dysfunction, implying a “normal,” non-dysfunctional, or functional,
account of female orgasm when there is no single accepted account of female orgasm as noted
above.
Adaptation 65
questions arises in the explanation of why so many miniaturized salamanders

have four toes, as you can see in Figure 4.3 of the independent lineages.
Let us examine now how a methodological adaptationist would analyze
this salamander example in Figure 4.3. We do not have to speculate:
Methodological adaptationists Reeve and Sherman have written about this
case, claiming that it may best be described as a case of natural selection,
under the assumption that certain test conditions are undertaken. They pro-
pose that either: “(1) the production of four toes minimally disrupts the
development of small individuals” or “(2) for small individuals, locomotion,
clinging, and foraging, for example, are more efficient with four than with
five toes” (1993, p. 22).
According to Reeve and Sherman, both hypotheses (1) and (2) are functional
explanations, which they prefer to the developmental constraint and phyletic
inertia explanation offered by Wake. They object that Wake has not explored
either one of these selective explanations. They find arguments based on trait
persistence to be “mysterious,” focused as they themselves are on obtaining
a function explanation. They propose what they call the “crucial” thought
experiment: “What would be the evolutionary result if a mutant alternative
trait arose and competed with the observed trait” (in this case, the four-toed
form)? This thought experiment sets the trait in the context of selection rather
than just development. This is, thus, for them, the “crucial” thought experiment
Figure 4.3 Independent four-toed lineages in the salamander family

Plethodontidae. Independent evolution of four-toed state in three separate
lineages (Wake 1991, p. 548, Figure 1).
precisely because they have only one type of answer in mind, a function answer,
one in the context of selection processes alone.
Let us take a look at this case using our logic of research questions framework.
Slotting their proposed questions into the options for functional accounts, as they
suggest, we get, as a set of answers to explain the convergence of multiple
lineages onto a four-toed miniaturized state:
BOX 4.6 METHODOLOGICAL ADAPTATIONIST RESEARCH QUESTION

What is the function of the four toes on the salamanders?
A: “The production of four toes minimally disrupts the development of small

individuals.”59
A: “For small individuals, locomotion, clinging, and foraging, for example, are
more efficient with four than with five toes.”60
Faulty and nonresponsive A: In contrast to functional answers, the

developmental and phyletic constraint answer is “mysterious.”61
But note that the first ‘function’ answer really is a developmental answer,
contrary to the initial claim of Reeve and Sherman, and not fully a function
answer after all. Because Reeve and Sherman have set up the problem using the
methodological adaptationist framework, their research question requires
a function answer as responsive.
We might say that the answer is minimally compatible with a function
answer. But it’s more, it’s actually what Wake and his colleague studied in
their lineages, and it is part of Wake’s proposal of a developmental and phyletic
constraint explanation.
According to Wake, who has spent decades studying these lineages of
lungless salamanders, which include all tropical salamanders, a total of
about 45 percent of the species of all salamanders, the answer may be a bit
of both factors (1991). The situation is this. Groups of descendent salamanders
are convergent if they have similar morphological but different ancestral
states.
One particularly important factor in their evolution is the very large
genome size of the salamanders, and the consequent large cell size and
slow cell cycles that result. They are the largest genomes of any terrestrial
vertebrate, with consequences for its morphology, such as the four-toe
59 60 61
Reeve and Sherman 1993. Reeve and Sherman 1993. Reeve and Sherman 1993.
Adaptation 67
limitation with small size. It is a situation of indirect mechanisms of selection

on body size: Large genome size is a selected mechanism for controlling body
size via slow cell division times. Moreover, selection for body size has an
incidental consequence of reduction of toe number. So, what looks like
selection directly on toe number is likely actually selection on body size via
slow cell division. And what seems to require adaptive explanations in cells
(i.e., large genome size) is likely another mechanism for controlling body
size. In sum, the connection is that large genome size results in slow cell
division, slow cell division results in a small number of cells, which results in
a small body size, and also because the slow process of cell division results in
the last-to-form elements of body parts (like the fifth toe) not forming at all
(Pers. Comm. J. R. Griesemer; Wake 1991).
Different branches of the salamander group independently have arrived at the
four-toed state, but they are nearly identical in structure and are produced by the
same complex of developmental options. As Wake writes, “[t]his is a direct
example of design limitations, in which alternative states are sharply defined”
(1991, p. 549). These are examples of how convergence can be a product of
“design limitations in the form of developmental constraints, which are only
indirectly related to adaptive processes.” Hence, selection for very small size
may have as an incidental side effect the reduction of a toe.
But Reeve and Sherman claim that all that Wake’s developmental and
phyletic constraints approach has to offer is a “description” but no
“explanation.”
As I understand scientific explanations, according to van Fraassen’s “prag-
matic theory of explanation” (1977), scientific explanations are answers to
“why questions.” As such, they provide the desired and sought-out information
to answer a scientific inquiry as a description. Thus, all scientific explanations
are descriptions in that they provide descriptions of systems or phenomena that
answer the specific question sought in a scientific inquiry or question.
But Reeve and Sherman contrast descriptive and explanatory claims. See
their dismissal of phyletic inertia as explanatory:
[‘phyletic’ inertia] is sometimes treated as a unique mechanism of trait

persistence. It is more appropriately regarded, however, as a descriptive
label for the evolutionary stasis of a trait. (1993, p. 18; their emphasis)
This is much easier to see when we use the alternative evolutionary factors
framework:
Comparing Boxes 4.6 and 4.7, the evolutionary factors approach makes very
clear the complementary nature of the selective and developmental constraints
explanations of the convergence of four-toedness in the salamanders.
BOX 4.7 EVOLUTIONARY FACTORS RESEARCH QUESTION

What evolutionary factors contribute to the form and distribution
of this trait?
Possible and Responsive Answers:
A: Smaller salamanders are selected in certain environments, pushing miniatur-

ization in many of the lineages (Selection)
A: Four toed-ness is constrained through genome size and cell size once miniatur-
ization of the lineage takes place (developmental and phyletic constraint).62
A: Other selective and developmental factors can come into play in this context.
We don’t have to take an approach like the methodological adaptationists where

the views are seen as competing or mutually exclusive, as Reeve and Sherman do.
And with the logic of research questions we can see precisely why they see some
answers as real explanations and some as “mysterious” or mere descriptions.
Reeve and Sherman write:
If structuralism is distinct from functionalism, it rests on unspecified – indeed

mysterious – mechanisms of trait persistence . . . In summary, the structuralist
approach either rests on a phenotype-set specification problem and therefore
is fundamentally flawed or it dissolves into the recognition of selective
developmental constraints, which is consistent with adaptationism and func-
tionalism. (Reeve and Sherman 1993 p. 21)
For them, the only “real” explanations are answers to the function questions, that is,
an answer is either “fundamentally flawed” or it is an explanation of adaptations.
Reeve and Sherman accuse the concept of a developmental constraint as
being “almost as vague as that of phylogenetic inertia,” which they savage in
their article (1993, p. 20).
Everything else is apparently merely a description, under their view, as we
can see with this salamander example. But Wake shows us that two answers –
the selective and the developmental constraint – can be compatible and inform-
ative, as we saw in Box 4.7, in the salamanders.
4.3 Bicoid: Novelty and the Case of the Hox Genes

The logical problems with the adaptationist methodology can be seen clearly in
the contrasts that we were just discussing. But we now turn to a case in genetics
that is perhaps more difficult to analyze, one involving the evolution of
a developmental gene of the famous and important Hox family, the genes
62
See Wake (2009) for analysis of the first two evolutionary factors mentioned here in the
salamander case working together.
Adaptation 69
responsible for placing segments and legs and heads in their correct places on
the body forms of an organism.
The Hox gene we will look at is called bicoid, and it is descended from its
ancestral gene, called zen, and they are both involved in determining where the
head will appear on the fruitfly. The challenge is that bicoid has recently rapidly
evolved from its ancestral gene, zen, and yet there seems to be no evidence for
selection forces to account for such a change straightforwardly, directly on the
bicoid gene (Carroll 2005).
One of the challenges for selection accounts of novel traits has to do with the
dynamics of the selection process itself. Selection processes excel at refining
traits to fit their local environments, but how do they come up with brand new
traits? In fact, they rely on outside sources of variation to select upon, as we
discussed in Section 2.5.
Moreover, one key thing to know in this example is that when natural
selection acts on genes, it usually restricts variation in the gene, because it
chooses the correct form of the gene and not the other forms (see Gannett
2010).
And I’m just using the “choosing” language here for convenience. The more
strongly selection acts, the narrower the range of variation of the gene becomes.
Likewise, the more relaxed the selective forces on a gene, the more variation
accumulates in and surrounding the gene. When a gene is not expressed, it can
vary more because selection is not acting to reduce the variation in the gene. As
selective constraint is relaxed on a gene, natural variability in the gene is thereby
increased, and we expect an increase proportional to the measure of the relax-
ation of selection on the gene. However, this may depend on the abundance of
variation for a given trait. When selection is weak, different traits may vary at
different rates. Thus one cannot simply infer the strength of selection from the
amount of variation present. But we can make the reverse inference: Less
selection means more variation in the bicoid gene.
In addition, while most genes are expressed by the complete zygote – the
paired egg and sperm, which contains both the mother’s and the father’s cells –
some genes are expressed only in the cells of the mother, called ‘maternally
expressed’ genes (Barker et al. 2005).
Under maternally expressed genes, only half as much selection is taking
place on the cell through the father’s genes, which are not expressed at all, so
they are twice as diverse as regular zygotic genes because of selection acting
only on the mother’s side. With zygotic selection, both the mother’s and the
father’s genes are being selected, so we get narrowing of variability on both
sides. But with maternally expressed genes, when only the mother’s genes are
being selected, we get increased variation of the father’s genes, because they are
not undergoing selection. We could say that the father’s genes are “sheltered
from selection forces” by the maternally expressed genes, because they are not
being screened by natural selection. A selective death owing to genes in the
zygote is twice as selective (it undergoes selection twice as strong) as a selective
death of a zygote owing to genes in its mother.
With this increased diversity produced by maternally selected genes and the
resultant expansion of variability on the father’s genes, the genes can evolve, or
diverge between populations or species more quickly, than the genes in the regular
zygotic context, under which there is no advanced or accelerated variation. Such
relaxed selection (on the father’s genes) creates more divergence between popu-
lations and species than ordinary zygotic adaptive purifying selection does.
Despite the fact of increased genetic diversity because of maternally expressed
genes and the accompanying relaxed selection, methodological adaptationists
assume that bicoid must be adaptive in its evolution. Nevertheless, the increased
genetic diversity arising from maternally expressed genes can explain their rapid
evolution compared to the regular, zygotically expressed form, the ancestral zen
form, as a live alternative to the adaptive account.
Michael Barker, Jeffrey Demuth, and Michael Wade (2005) performed an
experiment on this type of maternally expressed selection that explained the
evolution and selection of the bicoid and zen Hox genes in fruit flies. Population
genetic theory predicts relaxed selection on maternally expressed genes with
sex-limited expression, as we just discussed. They performed a series of
experiments to investigate whether this phenomenon showed up in laboratory
species of fruit fly, measuring variation and the expected accelerated evolution
in the flies in the lab just as was predicted by theory.
Is any of this presentable using the terms we’ve been discussing so far? Can
the methodological adaptationists handle this case? Does the evolutionary
factors approach do better? Let us start by asking the methodological adapta-
tionist question of the bicoid gene.
The Methodological Adaptationists’ Research Question is: “What is the
function of this trait?” In one sense, there is an obvious and obviously correct
answer to this question put just so, which is: “the function is to put the head in
place,” as we get in Box 4.8.
An adaptationist might be completely satisfied with this answer, but usually,
such an answer about function needs to be accompanied by an adaptive evolu-
tionary account of the trait, saying how the trait was favored by selection
through the evolutionary process, as shown in Box 4.9.
But is there such an account to be offered in this case? Again, one problem with
selective accounts involving novel traits like bicoid here is that selection is really
strong at providing adaptationist explanations about repurposing traits or revising
Adaptation 71

What is the function of this trait?
A: The function of this trait is to put the head in place.

Etc.
BOX 4.9 METHODOLOGICAL ADAPTATIONIST RESEARCH QUESTION: WHAT IS THE

FUNCTION OF THIS TRAIT?
A: The function of this trait is to put the head in place.

Full A: This trait has this function and correlation with fitness, and was selected
through the evolutionary process, and we offer the following account to explain
the history and selection of this trait.
them, but not so good at explaining novel traits, as we discussed in Section 2.5. In
fact, questions concerning novel traits can rarely be satisfied with straightforward
selective explanations, precisely because selection is usually about selecting,
trimming, and revising something, and not about inducing something new.
A significant part of the question about this trait concerns how such an important
trait so recently appeared and rapidly changed relative to the rest of its genome.
What is the evolutionary story behind the rapid evolution of this trait?
Does it help to turn to the evolutionary factors approach here?
What does the Barker, Demuth, and Wade story give us that goes beyond the
function of the trait? They appeal to sex-limited selection in maternal effect
genes having twice as much variation as zygotically expressed genes to account
for the speedier evolution of the maternal-effect gene, bicoid, which controls the
orientation and placement of the head in the body. Such an account cannot be
arrived at through selection alone, as relaxed constraint on selection plays the
key role in producing the increased variation in the maternally expressed genes.
Such relaxed selection induces increased variation and novelty. Adaptation and
natural selection work against novelty, hence, adaptive explanations can only
explain the kind of novelty that results from refinement, and not this kind of
novelty, which results from the relaxation of selective constraint.
Ultimately, this means that methodological adaptationist logic limits the
types of traits that we can give adequate answers to, and forces us toward
certain sorts of novelty and away from other sorts, those reliant on true increases

What evolutionary factors account for the form and distribution
of this trait?
A: Maternally expressed genes produce increased genetic variability through

suppression of selection on the father’s genes (easing of selection and increase
in genetic variability).
A: Increased genetic variability produces wider genetic constraints controlling the
field of exploration (constraints).
A: Wider constraints allow innovation and novelty in the bicoid gene (develop-
ment and novelty, mutations).
in variation. Zygotic selection allows only winnowing selection on ancestral zen

genes, that is, it allows repurposing only, as novelty. We must turn to the other
evolutionary factors in order to account for the profound kind of novelty seen in
this case, involving more than refinement of past cases. We are left needing to
appeal to processes other than natural selection, which requires selecting from
our list of other factors in the evolutionary factors approach. The adaptationist
approach is limiting precisely by requiring the trait to be a repurposing only,
otherwise the approach cannot fully explain it.
In other words, positive selection does not work as the key factor in the hard
case that goes beyond the kind of novelty involving refinement of past traits, so
we must turn to the other evolutionary factors of development and constraint,
and as here, sex-limited traits arising from developmental factors. Constraints
on selection are serving as a novelty-producing factor in this case. This is shown
through predictions from population genetics and confirmation of those predic-
tions through experimental data. In sum, this is an instance where methodo-
logical adaptationism’s shortcomings are on display in a subtle but decisive
manner, in showing how the significant factor of evolutionary novelty is not
fully accounted for within that approach. Compare Boxes 4.9 and 4.10.
4.4 How Methodological Adaptationists Got Exaptation Wrong63

4.4.1 Background
There is one final type of evolutionary factor to consider before we close our
consideration of adaptation. In 1982, Stephen Jay Gould and Elisabeth Vrba
coined a new term, “exaptation,” to mean a trait that contributes to fitness but
63
“Exaptation Revisited: Changes Imposed by Evolutionary Psychologists and Behavioral
Biologists,” Biological Theory 12, pp. 50–65 (2017). E.A. Lloyd and S.J. Gould.
Adaptation 73
was not selected to do so. It was meant to contrast with “adaptation” (see
Table 1.1). They also said that any trait that contributes to current fitness is an
“aptation,” which encompassed both adaptations and exaptations. The skull
sutures in human babies (Figure 2.2) are a perfect example of an exaptation;
they contribute to fitness, without having been built by selection for that purpose,
that is, they are something with “vital current utility based on a cooptation of
structures evolved in other contexts and for other purposes (or perhaps for no
purpose at all)” (Gould 1991, p. 46). In other words, we have a trait that does not
vary within the population, such as the existence of skull sutures in mammals, but
which increases fitness over possible (but never actual) alternative traits, such as
not having any skull sutures. If there had ever been significant variation in skull
sutures, they would be selected against during birth, but there is not, so they are
neither engineering nor selection-product adaptations. But they do contribute to
fitness in mammals, in easing birth, so they are “aptations,” with no history of
selection, since baby skull sutures are just like reptile skull sutures, products of
developmental constraint or architecture.
Exaptations became significant in a debate within evolutionary psychology in
the early and mid-1990s, primarily because of an intervention by Gould, who
claimed that many brain activities were likely to be exaptations – that is, effects
that contribute to fitness, but were not selected to do so – rather than genuinely
selected evolutionary functions in both the etiological and engineering sense.
This went against the orthodoxy of evolutionary psychology at the time,
which was led by methodological adaptationists and was more inclined toward
interpreting obviously fitness-increasing brain activities as evolutionarily
selected functions.64
Unfortunately, in the context of that debate, Gould made an error of speaking
and used the term “function” in the vernacular, or commonsense, manner, rather
than in the technical, evolutionary engineering sense, as we shall see in a moment.
Later on, some methodological adaptationists mistakenly took this occasion of
Gould’s misspeaking as confirmation that ‘exaptation’ had an evolutionarily
‘designed’ function and was a version of an engineering adaptation. This was
a mistake because exaptation is not a version of adaptation; it is a distinct form of
aptation. As a result, other methodological adaptationists provided a standard of
evidence for exaptation that was inappropriate and based on an adaptationist
(This section of the Element, and the paper it is based on, were first written with Stephen Jay
Gould as my co-author in the spring of 2002. All of the sections were drafted before he passed
away in May 2002. It was our third co-written paper. I left it alone for over ten years, until
I finally realized that he would have liked our arguments to be published, so I updated and
completed the manuscript on my own. I would like to acknowledge Steve’s contributions to this
section, both conceptual and structural.)
64
See, for example, Tooby and Cosmides (1997) debating Gould in the New York Review of Books.
worldview. These ideas have been rendered practically useless through their
mistaken definitions and misapplications by some evolutionary psychologists
over these last decades.
4.4.2 Evolutionary Function, a Misspoken Phrase, and a Misunderstanding

Various discussions of Gould and Vrba’s (1982) concept of ‘exaptation’ have
been plagued by terminological ambiguity. Specifically, varying uses of the
concepts of ‘current utility’ and ‘function’ have contributed to uncertainty about
when and how the notion of ‘exaptation’ should be used (see Table 1.1 for
definitions). In this section, I shall focus on the issue of exaptation as it is
discussed in two characteristic, widely cited, and very influential papers by
David M. Buss, Martie G. Haselton, Todd K. Shackelford, April L. Bleske, and
Jerome C. Wakefield (1998)65, and Paul W. Andrews, Steven W. Gangestad, and
Dan Matthews (2002a)66.
In a widely cited paper aimed at explaining to psychologists the concepts of
‘adaptation,’ ‘exaptation,’ and ‘spandrels,’ David Buss and colleagues (1998)
attempt to delineate the meanings and evidential requirements of these three
terms. The notion of ‘function’ plays a central role in their analysis. In discuss-
ing adaptations, they write, “to propose that a trait is an adaptation is to propose
that it was designed by natural selection in past environments to serve some
function” (emphasis added; 1998, p. 85). Thus, they are using the same notions
of function and adaptation we introduced in Section 1.
Now let us look at the way that Gould and Vrba used the term ‘function’ in their
discussions of exaptation. The term ‘exaptation’ applies to two types of traits:
1. Traits that were adapted for one evolutionary function but were later co-
opted (but not selected) to serve a different role; and
2. Traits that were correlates of growth, or accidental by-products, or “span-
drels,” that were later co-opted (but not selected) to serve another role.
Gould and Vrba also follow George Williams’ terminology regarding func-
tion, stating that “the operation of an adaptation is its function,”67 just as we find
in Section 1. Similarly, the operation of a useful character not built by selection
for its current evolutionary role is an “effect.” Exaptations’ effects do contribute
to current fitness, by definition, but are not designed or selected to do so.
“Adaptations have functions; exaptations have effects” (Gould and Vrba
1982, p. 6; emphasis added).
65
Cited by 914 on Google Scholar, accessed June 2, 2020.
66
Cited by 334 on Google Scholar, accessed June 2, 2020.
67
Original emphasis; Gould and Vrba 1982, p. 6.
Adaptation 75
Gould and Vrba also suggest that the general phenomenon of being fit for
a specific evolutionary role (current fitness) should be called ‘aptation’ rather
than the usual ‘adaptation’. This allows for a distinction between traits selected
for the current role, and those not. The most important part of these definitions is
that exaptations must contribute to present fitness, but were not selected,
historically, to do so. This is as opposed to adaptations that also contribute to
present fitness, but which were naturally selected for their contributions to
fitness and evolution of an adaptation in the past.
The regular requirements for adaptations demand that an adaptive account
explain the adaptive feature(s) or modification(s) acquired through the selective
process over time, its ‘engineering’ history of its complex and built-up adaptive
traits. Under these definitions, both adaptations and secondary adaptations have
selective histories, but exaptations do not. Recall that this definition of adapta-
tion contrasts to the “product of selection” definition.
Note here that there is an important distinction to be made between second-
ary adaptations, which can be maintained by directional, stabilizing, or other
forces of selection, and exaptations, which are not primarily maintained by
selection. Stabilizing selection is therefore not the primary explanation of
stability in the trait. Rather, exaptations maintain their status primarily
through other biological mechanisms, such as developmental constraints,
embryological considerations, or other structural means such as by-products
or genetic correlations. The claim is: Selection is not the evolutionary cause
that is maintaining the trait where it is.68
Significantly, exaptations can be modified by selection to serve yet a new
evolutionary function: to become “secondary adaptations.” For example, fea-
thers originally served as exaptations for flight, under the assumption that they
originally evolved for thermoregulation of the dinosaurs they appeared on. It is
hypothesized that they were then utilized for short flights. However, the various
subsequent modifications of feathers for flight are secondary adaptations, thus
making certain features of the feathers engineering secondary adaptations
themselves (Gould and Vrba 1982, p. 11). Contrary to a common objection, it
is not the case that one generation of use in flight makes the feathers an
engineering secondary adaptation, which requires generations of genetic
change and distribution of that genetic change throughout the populations of
the species. Only after such distributed genetic change and the acquisition of
such genetic change and adaptive features by members of the species is the
feather considered to be an engineering secondary adaptation for flight.
68
E.g., Linde-Medina 2011; Newman & Bhat 2011; Amundson 2005.
Thus, if there is a stable trait in the population that contributes to fitness, on its
face, it might be either an adaptation or an exaptation; it is simply an “aptation.”
It might have arrived at its present state through a selection process, in which
case it is either a primary or a secondary adaptation. It may also have attained its
current identity primarily through embryological or developmental constraints,
and other structural features. The point is that these can explain why it is stable
in the population, as an alternative and complement to stabilizing selection or
other forces of selection. Relevant mechanisms might include genetic con-
straints and developmental details of the organism, correlations of growth,
and by-products of other features of the organism. For example, the constancy
of having seven cervical vertebrae in mammals, including mice, humans, and
giraffes, has been revealed as a product of the involvement of Hox genes
(related to the Bicoid case) and developmental constraints (Galis 1999).
Take the case of a novel use of a trait in a fitness-enhancing way. For example,
an insect allele that was neutral before but in a new context provides protection
against a novel pesticide would be, in the first exposure, not a selection-product
or engineering adaptation for resistance until it undergoes natural selection (i.e.,
differential reproduction relying on this allele’s protection). After selection, it
would be considered a selection-product adaptation, as there is no new machin-
ery or built-up trait involved in the process, but rather simple differential
survival of the alleles (Lloyd 2001).
When Buss and colleagues confuse evolutionary “function” with exaptation’s
effects, they ignore this important point.
4.4.3 The Difference between Function and Effect
In a 1991 paper, Gould was not completely careful in separating “function” and
“effect,” and his misspeaking has led to a great deal of confusion. The occasion of
the confusion was that Gould once described exaptation as “a feature, now useful
to an organism, which did not arise as an adaptation for its present role, but was
subsequently co-opted for its current function” (1991, p. 43, my emphasis). Here,
Gould misspeaks and does not use “function” to refer strictly to the activity of an
engineering adaptation. He instead uses “function” in a more vernacular sense so
that it misleadingly appears to signify the useful action of a selected trait. Gould
makes clear that such action involves enhancing current fitness (1991, p. 47).
This combination of statements led Buss and colleagues, due to their adapta-
tionist biases, to conclude that an exaptation must have a “function” in the
stricter, adaptive sense (1998, p. 539). Buss and colleagues end up confusing the
requirement that exaptations contribute to current fitness with their own, added
requirement that they serve a “function,” understood as a solution to an adaptive
Adaptation 77
problem. What is at stake in the confusion is the relative importance of using

natural selection versus other evolutionary factors to account for currently
useful, ‘aptive,’ fitness-enhancing traits, and in general, the overall power of
adaptive explanations.
They contrast selective functions, which for Buss et al. include exaptations, with
“biologically functionless uses,” which they refer to as “effects,” “consequences,”
or “byproducts” (1998, p. 539). Thus, they have severely altered Gould and Vrba’s
terminology when they exclude “effects” from the performance of exaptations.
These effects are precisely what Gould and Vrba defined as the outcomes of
exaptations! What Buss and colleagues have described here are, in fact, secondary
adaptations, not the original nonadaptations that signify “exaptations.”
4.4.4 Applying the Logic of Research Questions
Let’s look at this using the Logic of Research Questions.

As we can see, Buss and colleagues have mistakenly turned a nonresponsive
answer, the true exaptationist position, into a responsive answer that satisfies
their function research question (See Box 4.11, below). As such, the actual
definition of ‘exaptation’ is missing and is not being actively considered by the
evolutionary psychologists under their research question in a paper that has
been cited over 900 times.
The alternative, “Evolutionary Factors” research question, offers the full
variety of evolutionary explanations, including adaptation through selection,
exaptation through cooptation (under the original definition), and so on. These
questions and a few of their answers can be seen in Box 4.12.

“What is the function of this trait?”
A: This trait has the function F, an adaptation.

A: This trait has the function G . . .
A: *This trait has the function H as an exaptation, as a result of a process of
selection* (*Under Buss and colleagues’ mistaken assumption that exaptations
have functions, and are products of selection)
Missing Nonresponsive A: This trait does not have a function, and is an exaptation,
as a result of a process of co-optation under Gould & Vrba’s definition (i.e.,
nonresponsive to the function question, under the true definition of exaptation,
where exaptations do not have functions, but rather only effects, a “null” result
according to the adaptationists).
Nonresponsive A: This trait is a by-product of selection on another trait (non-
responsive to the function question, a “null” result according to the adaptationists).

“What evolutionary factors account for the form and distribution of
this trait,” for example, or, “Does this trait have a function?”
Possible Answers:
A: This trait occurs in the population because it has the function F (i.e., the trait is
an engineering adaptation or secondary adaptation).
...
...
A: This trait has its current form and distribution because it is an exaptation as
a result of co-optation but not selection (cannot be combined with the first two
adaptation answers, unless the traits are different).
A: This trait has its current form and distribution because of some combination of
the above factors.
Etc.
Under the evolutionary factors approach, exaptation is one possible answer

to the question “What evolutionary factors account for the form and distribu-
tion of this trait?”, and it appeals to a process of cooptation in contrast to
a process of selection.
Buss and colleagues misleadingly discuss the sources or mechanisms of co-
optations of structures, under their faulty definition, discussed above. In con-
sidering birds’ feathers, which were originally evolved for thermoregulation but
subsequently co-opted for flight, they write “it is clearly natural selection that is
responsible for transforming an existing structure into a new, modified structure
with a different function” (1998, p. 541). But Buss and colleagues have con-
flated two processes here. They’ve taken one process in which feathers, without
physiological modification, were co-opted for flight through use (an exapta-
tion), and confused it with another in which feathers were subsequently adap-
tively modified for enhanced flight capability (a secondary engineering
adaptation, which has a function in both the etiological and design sense).
They object to Gould’s use of some mechanisms of co-optation, like cogni-
tive capacities and motivational mechanisms, because they are clearly not cases
of natural selection. They are at pains to distinguish current uses that are not
“co-opted by natural selection” for their current uses from those that are
naturally selected. But that is the whole point of introducing “exaptation.”
Buss and colleagues fail to see that Gould does not require that the trait be “co-
opted” by natural selection (which really means “selected,” based on their use
of the term) in order to be an exaptation; this is a result of their own collapse of
the two processes of exaptation and secondary adaptation.
Adaptation 79
Some measure of the responsibility for this confusion is Gould’s. His single
misspeaking involving the term “function” in the 1991 paper was seized on by
Buss and colleagues, and led them to search for an original function and
a “distinct later function” in secondary adaptations, their “exaptations” (1998,
p. 541). When finding no later adaptive function, Buss and colleagues conclude
that something is amiss. Moreover, when they understand exaptations as arising
from earlier functions, they are missing half of the definition of exaptation, in
which many traits with current uses are derived from traits with no adaptive
function at all (i.e., spandrels).
But what turns on this confusion? The answer becomes clear in Buss and
colleagues’ discussion of the evidence required to show that something is an
exaptation. They require specification of (1) the original adaptation or by-
product that was later coopted for the exaptation; (2) the causal mechanism
responsible for the co-opting (e.g., on their account, natural selection or
a selective motivational mechanism; note that they do not include any devel-
opmental constraints or mechanisms or nonselective factors); and (3) “the
exapted biological function” of the trait, “that is, the manner in which it
contributes to the solution to an adaptive problem of survival or reproduction”
(1998, p. 542).
Here, Buss and colleagues’ notion that an exaptation must have a biological
function is doing some real work. As they put it, both the concepts of exapta-
tion and adaptation invoke function, “therefore, both must meet the concep-
tual and evidentiary standards for invoking function.” It becomes clear that
these standards are much too strict to bear the weight of what Gould and Vrba
have defined as exaptations. Buss and colleagues write, for example, that the
criteria for a proposed function include “the hallmarks of special design,
including specialization of function, for solving a particular adaptive prob-
lem” (1998, p. 546). Thus, it seems that Buss and colleagues are using
Williams’ engineering definition of function and are mistakenly assuming
that exaptations must exhibit this kind of function, whereas exaptations are
actually demarcated precisely to avoid such a burden.
Buss and colleagues claim that selectionist explanations “would generally be
necessary for explaining how functionless by-products are transformed into
coopted spandrels that perform specific functions,” thus making complete their
mistaken view of the connection between function and co-optation. In an
adaptationist spin, all of this is used to defend their sought-for conclusion that
natural selection is “the basic explanatory principle in biology” (1998, p. 543;
emphasis added).
The key problem is that their view does not allow for exaptation to serve its
original role in evolution, as a potential alternative evolutionary factor, since it
has been defined away as a selective scenario, often involving stabilizing

selection. Thus, the differences between the evolutionary psychologists Buss
and colleagues, and Vrba and Gould are clear, as we can see from the Logic of
Research Questions.
It is badly mistaken to read exaptations as examples of secondary adaptations
subject to stabilizing selection. Because methodological adaptationists, like
Buss and colleagues, ask the “function” research question, their question
needs a function answer, thus producing a function-based definition of exapta-
tion. This is incorrect. In sum, Gould’s single, misspoken mention of the
‘function’ of an exaptation in his 1991 paper has enabled Buss and colleagues
to completely reverse the intended meaning of ‘exaptation.’
A similar problem arises with evolutionary psychologists Andrews et al.
(2002a, 2002b). In a paper in which they claim to define exaptation and
propose definitive standards of evidence for adaptation and exaptation, they
assume adaptations and functions for traits at the beginning of inquiry, pro-
posing that all adaptive accounts must be eliminated as alternatives before
a nonadaptive account may be seriously considered (Andrews et al. 2002a
p. 534; 2002b p. 504). This approach suffers from similar faults as Buss
et al.’s, but we won’t detail it here; analysis can be found in Lloyd and
Gould (2017).
4.5 Conclusion
Before we end this discussion of the risks or shortcomings of methodological
adaptationism, I must acknowledge that many will object to my critique of
adaptationism: “But methodological adaptationism is so useful! Surely you are
not advocating sacrificing our most fruitful research tool?!”
And no, I am not doing so, since the evolutionary factors framework includes
the use of adaptation, and the search for connections to fitness, function, and
“design” may even serve as a first “go-to” algorithm.
The evolutionary factors framework may advocate starting69 research by
trying out the adaptive answer to “Does this trait have a function?” and
learning and keeping at the top of the mind as real causal alternatives the
other evolutionary factors. (Sometimes this different set of answers may
require a different laboratory setup or tools, e.g., David Wake’s work on
salamanders.70) That is the difference between methodological
69
Of course, different researchers may start with different questions. My point is that typical
researchers in animal behavior, evolutionary psychology, etc., will likely want to start by
searching for adaptations of a given trait, and they can still do so under the evolutionary factors
approach.
70
Wake 1991, 2009; Griesemer 2013, 2015; Wagner 2000.
Adaptation 81
adaptationism and the evolutionary factors framework: The nonadaptive

explanations are real, causal, live alternatives that can be supported with
evidence. Moreover, this evidential support for the full variety of evolution-
ary factors must be recognized when it is presented, and not treated within
a mutually exclusive framework of evidence.
To reiterate, I am not in any way against adaptive explanations themselves.
But I have highlighted some risks of a very popular approach to research into
evolutionary causes. These dangers become obvious when we examine the logic
of the research questions and their relevant answers, within the methodological
adaptationist approach and the contrasting evolutionary factors framework.
When a research approach makes any particular types of hypothesis especially
difficult to entertain or accept, it deserves serious scrutiny. Keeping the logic of
the research questions in mind when dealing with the scientific errors commit-
ted by adaptationists allows us to analyze and explain them straightforwardly.
The presence of researchers like Symons, Wade, or Wake, who engaged in their
research using the more inclusive evolutionary factors methodology, exempli-
fies a living available alternative method.
Evolutionary adaptations are fascinating aspects of living beings.
Understanding not just whether to study them, but also how to study them, is
crucially important to the success of evolutionary science.71
71
Suggested Further Reading: For evidence for by-product/bonus account of female orgasm, see
Lloyd 2005a and Levin 2014; for the hereditary basis of orgasm, see Dawood et al. 2005 and
Dunn et al. 2005; for total lack of any genetic correlation with fitness, see Zietsche and Santtila
2011, 2013. See Marlene Zuk (2006) for a review of my 2005 book; see Dixson 2012 for the
authoritative study of primate sexuality, including comparative study of human beings; see Wake
1991, 2009 for more on the salamander case. See Barker et al. 2005 for more on the Bicoid, Zen,
and Hox genes.
References
Ackerly, D. D. 2004. “Adaptation, niche conservatism, and convergence:
Comparative studies of leaf evolution in the California chaparral.” The
American Naturalist 163(5): 654–71. https://doi.org/10.1086/383062
“Adaptive evolution | boundless biology.” n.d. Accessed November 28, 2018.
https://courses.lumenlearning.com/boundless-biology/chapter/adaptive-evo
lution/.
Airoldi, G., 2018. “More than fitness. A robustness-based proposal of a logical
space to classify processes behind evolutionary phenomena.” Kairos.
Journal of Philosophy & Science 20(1): 89–112.
Alcock, J. 1987. “Ardent adaptationism.” Natural History 96(4): 4.
Alcock, J. 1998. “Unpunctuated equilibrium in the natural history essays of
Stephen Jay Gould.” Evolution and Human Behavior 19(5): 321–36. https://
doi.org/10.1016/S1090-5138(98)00029–4.
Allen, C. 2002. “Real traits, real functions?” In Ariew, A., R. Cummins, and
M. Perlman (eds.) Functions: new essays in the philosophy of psychology and
biology. New York: Oxford University Press. 373–89.
American Psychiatric Association. 2013. “Sexual dysfunctions” in Diagnostic
and statistical manual of mental disorders (5th ed.). Washington, DC. https://
doi.org/10.1176/appi.books.9780890425596.dsm13
Amundson, R. 1994. “Two concepts of constraint: Adaptationism and the
challenge from developmental biology.” Philosophy of Science 61(4):
556–78. https://doi.org/10.1086/289822
Amundson, R.. 1998. “Typology reconsidered: Two doctrines on the history of
evolutionary biology.” Biology and Philosophy 13(2): 153–77. https://doi.org
/10.1023/A:1006599002775
Amundson, R. 2001. “Adaptation and development: On the lack of common
ground.” In Orzack, S., and E. Sober (eds.). Adaptationism and optimality.
Cambridge University Press, New York. 303–34.
Amundson, R. 2005. The changing role of the embryo in evolutionary thought:
Roots of Evo-Devo. Cambridge University Press.
Andrews, P. W., S. W. Gangestad, and D. Matthews. 2002a. “Adaptationism,
exaptationism, and evolutionary behavioral science.” Behavioral and Brain
Sciences 25(4): 534–47. https://doi.org/10.1017/S0140525X02530090
Andrews, P. W., S. W. Gangestad, and D. Matthews. 2002b. “Adaptationism –
how to carry out an exaptationist program.” The Behavioral and Brain
Sciences 25(4): 489–504.
References 83
Aoki, K. 1984. “A population genetic model of the evolution of oblique cultural

transmission.” Proceedings of the Japan Academy, Series B 60(8): 310–13
Aoki, K. 1986. “A stochastic model of gene-culture coevolution suggested by
the ‘culture historical hypothesis’ for the evolution of adult lactose absorp-
tion in humans.” Proceedings of the National Academy of Sciences 83(9):
2929–33.
Arnold, S. J. 1994. “Is there a unifying concept of sexual selection that applies
to both plants and animals?” The American Naturalist 144: S1–12. https://doi
.org/10.1086/285650
Baker, R. R., & Bellis, M. A. 1993. “Human sperm competition: ejaculate
manipulation by females and a function for the female orgasm.” Animal
Behaviour 46(5): 887–909.
Barash, D. 2005. “Let a thousand orgasms bloom [Book Review of The case of
the female orgasm. E. A. Lloyd].” Evolutionary Psychology 3(1): 347–54.
https://doi.org/10.1177/147470490500300123
Barash, D. P., and J. E. Lipton. 2009. How women got their curves and other
just-so stories: evolutionary enigmas. Columbia University Press.
Barker, M. S., J. P. Demuth, and M. J. Wade. 2005. “Maternal expression relaxes
constraint on innovation of the anterior determinant, bicoid.” PLoS Genetics
1(5): e57. https://doi.org/10.1371/journal.pgen.0010057
Beatty, J. 1987. “Natural selection and the null hypothesis.” In J. Dupre (ed.)
The latest on the best: essays on evolution and optimality. 53–75. The
Massachusetts Institute of Technology Press.
Boyd, R., and P. J. Richerson. 2009. “Culture and the evolution of human
cooperation.” Philosophical Transactions of the Royal Society of London
B: Biological Sciences 364(1533): 3281–88. https://doi.org/10.1098/rstb
.2009.0134.
Buss, D. M., M. G. Haselton, T. K. Shackelford, A. L. Bleske, and
J. C. Wakefield. 1998. “Adaptations, exaptations, and spandrels.” American
Psychologist 53(5): 533–48. https://doi.org/10.1037/0003-066X.53.5.533
Carroll, S. B. 2005. Endless forms most beautiful: the new science of evo devo
and the making of the animal kingdom. W. W. Norton.
Cavalli-Sforza, L., and M. W. Feldman. 1973. “Models for cultural inheritance.
I. Group mean and within group variation.” Theoretical Population Biology
4(1): 42–55.
Cavalli-Sforza, L. L., and Feldman, M. W. 1981. Cultural transmission and
evolution: A quantitative approach. Princeton University Press.
Charnov, E. L., and G. A. Parker. 1995. “Dimensionless invariants from foraging
theory’s marginal value theorem.” Proceedings of the National Academy of
Sciences 92(5): 1446–50. https://doi.org/10.1073/pnas.92.5.1446
84 References
Cheng, H., and W. M. Muir. 2005. “The effects of genetic selection for
survivability and productivity on chicken physiological homeostasis.”
World’s Poultry Science Journal 61(3): 383–97. https://doi.org/10.1079
/WPS200464
Chevalier-Skolnikoff, S. 1974. “Male-female, female-female, and male-male
sexual behavior in the stumptail monkey, with special attention to the female
orgasm.” Archives of Sexual Behavior 3(2). 95–116.
Cosmides, L., and J. Tooby. 1994. “Better than rational: evolutionary psych-
ology and the invisible hand.” The American Economic Review 84(2):
327–32.
“Cranial sutures and fontanels.” n.d. Mayo Clinic. Accessed December 5, 2018.
www.mayoclinic.org/diseases-conditions/craniosynostosis/multimedia/cra
nial-sutures-and-fontanels/img-20006785
Cummins, R. 1975. “Functional analysis.” The Journal of Philosophy 72(20):
741–65. doi:10.2307/2024640
Darwin, C. 1859. On the origin of species by means of natural selection, or
preservation of favoured races in the struggle for life. London: John
Murray.
Darwin, C. 1871. The descent of man and selection in relation to sex. London:
John Murray.
Dawood, K., K. M. Kirk, M. J. Bailey, P. W. Andrews, and N. G. Martin. 2005.
“Genetic and environmental influences on the frequency of orgasm in
women.” Twin Research and Human Genetics 8(1): 27–33. https://doi.org/10
.1375/twin.8.1.27.
Delph, L. F., and T. Ashman. 2006. “Trait selection in flowering plants: How
does sexual selection contribute?” Integrative and Comparative Biology
46(4): 465–72. https://doi.org/10.1093/icb/icj038.
Delph, L. F., and C. R. Herlihy. 2012. “Sexual, fecundity, and viability selection
on flower size and number in a sexually dimorphic plant.” Evolution:
International Journal of Organic Evolution 66(4): 1154–66. https://doi.org
/10.1111/j.1558-5646.2011.01510.x
Dewsbury, D. A. 1992. “Essay on contemporary issues in ethology: on the
problems studied in ethology, comparative psychology, and animal
behavior.” Ethology 92(2): 89–107. https://doi.org/10.1111/j.1439-0310
.1992.tb00951.x
“Digital morphology at the University of Texas.” n.d. Accessed December 5,
2018. http://digimorph.org/index.phtml
Dixson, A. 2009. Sexual selection and the origins of human mating systems.
Oxford University Press.
Dixson, A. 2012. Primate sexuality. 2nd ed. Oxford University Press.
References 85
Douglas, A. E., and J. H. Werren. 2016. “Holes in the hologenome: Why

host-microbe symbioses are not holobionts.” MBio. 7(2).10.1128/
mBio.02099–15
Dunn, K. M., L. F. Cherkas, and T. D. Spector. 2005. “Genetic influences on
variation in female orgasmic function: a twin study.” Biology Letters 1(3):
260–63. https://doi.org/10.1098/rsbl.2005.0308
El-Sabaawi, R. W., E. Zandonà, T. J. Kohler, M. C. Marshall, J. M. Moslemi,
J. Travis, A. López-Sepulcre, R. Ferriere, C. M. Pringle, S. A. Thomas, and
D. N. Reznick. 2012. “Widespread intraspecific organismal stoichiometry
among populations of the trinidadian guppy.” Functional Ecology 26(3):
666–76. https://doi.org/10.1111/j.1365-2435.2012.01974.x
Endler, J. A. 1978. “A predator’s view of animal color patterns.” In Hecht M. K.,
W. C. Steere, and B. Wallace (eds.), Evolutionary Biology. Evolutionary
Biology, vol II. Springer, Boston. https://doi.org/10.1007/978-1-4615-6956-5_5
Endler, J. A. 1986. Natural selection in the wild. Princeton University Press.
Fairbanks, D. J., and B. Rytting. 2001. “Mendelian controversies: a botanical
and historical review.” American Journal of Botany 88(5): 737–52.
Feldman, M. W., and K. N. Laland. 1996. “Gene-culture coevolutionary
theory.” Trends in Ecology & Evolution 11(11): 453–57.
Feldman, M. W., and L. Cavalli-Sforza. 1985. On the theory of evolution under
genetic and cultural transmission with application to the lactose absorption
problem. Stanford Institute for Population and Resource Studies.
Fisher, S. 1973. Understanding the female orgasm. New York: Basic Books
Fitelson, B., 2001. “A Bayesian account of independent evidence with applica-
tions.” Philosophy of Science 68(S3): S123–S140.
Freud, S. [1905] 1953. “Three essays on the theory of sexuality.” In The
standard edition of the complete psychological works of Sigmund Freud,
volume VII (1901–1905): A case of hysteria, three essays on sexuality and
other works. 123–246.
Freud, S. [1923] 1963. “Freud: introductory lectures on psychoanalysis.” The
standard edition of the complete psychological works of Sigmund Freud.
Futuyma, D. and M. Kirkpatrick. 2017. Evolution (4th ed.). Sinauer Oxford
University Press.
Galis, F. 1999. “Why do almost all mammals have seven cervical vertebrae?
Developmental constraints, hox genes, and cancer.” Journal of Experimental
Zoology 285(1): 19–26.
Gannett, L. 2010. “Questions asked and unasked: how by worrying less about
the ‘really real’ philosophers of science might better contribute to debates
about genetics and race.” Synthese 177(3): 363–85. https://doi.org/10.1007
/s11229-010-9788-1
86 References
Geary, D. C., and M. V. Flinn. 2001. “Evolution of human parental behavior and
the human family.” Parenting 1(1–2): 5–61. https://doi.org/10.1080
/15295192.2001.9681209.
Glymour, C. 1980. Theory and evidence. Princeton University Press.
Godfrey-Smith, P. 2001. “Three kinds of adaptationism.” In Orzack, S. and
E. Sober (eds.). Adaptationism and optimality. 344–62. Cambridge
University Press.
Gould, S. J. 1987a. “Freudian slip.” Natural History 96(2): 14–21.
Gould, S. J. 1987b. “Reply to Alcock.” Natural History 96(4): 4–6.
Gould, S. J. 1991. “Exaptation: a crucial tool for an evolutionary psychology.”
Journal of Social Issues 47(3): 43–65. https://doi.org/10.1111/j.1540-4560
.1991.tb01822.x
Gould, S. J. 2002. The structure of evolutionary theory. Harvard University
Press.
Gould, S. J., and E. S. Vrba. 1982. “Exaptation – a missing term in the science of
form.” Paleobiology 8(1): 4–15. https://doi.org/10.1017/S0094837300004310
Gould, S. J., and R. C. Lewontin. 1979. “The spandrels of San Marco and the
panglossian paradigm: a critique of the adaptationist programme.”
Proceedings of the Royal Society of London. Series B Biological Science
205(1161): 581–98. https://doi.org/10.1098/rspb.1979.0086
Griesemer, J. 2013. “Integration of approaches in David Wake’s model-taxon
research platform for evolutionary morphology.” Studies in History and
Philosophy of Science Part C: Studies in History and Philosophy of
Biological and Biomedical Sciences 44(4, Part A): 525–36. https://doi.org/10
.1016/j.shpsc.2013.03.021
Griesemer, J. 2015. “What salamander biologists have taught us about evo-
devo.” In Love, A. C. (ed.) Conceptual change in biology: Scientific and
philosophical perspectives on evolution and development. 271–301. Boston
Studies in the Philosophy and History of Science. Springer. https://doi.org/10
.1007/978-94-017-9412-1_13.
Griffiths, A. J. F., Wessler, R. C. Lewontin, W. M. Gelbart, D. T. Suzuki, and
J. H. Miller. 2005. An introduction to genetic analysis (8th ed.). Macmillan.
Griffiths, P. E. 1996. “The historical turn in the study of adaptation.” The British
Journal for the Philosophy of Science 47(4): 511–32. https://doi.org/10.1093
/bjps/47.4.511
Harrison, D. F. N. 1980. “Biomechanics of the giraffe larynx and trachea.” Acta Oto-
Laryngologica 89 (3–6): 258–64. https://doi.org/10.3109/00016488009127136.
Harrison, D. F. N. 1981. “Fibre size frequency in the recurrent laryngeal nerves
of man and giraffe.” Acta Oto-Laryngologica 91(1–6): 383–9. https://doi.org
/10.3109/00016488109138519
References 87
Hite, S. 1976. The Hite report on female sexuality. Bertelsmann.

Hosken, D. J. 2008. “Clitoral variation says nothing about female orgasm.”
Evolution & Development 10(4): 393–95. https://doi.org/10.1111/j.1525
-142X.2008.00247.x
Hrdy, S. B. 2005. “Cooperative breeders with an ace in the hole,” In Voland E.,
A. Chasiotis, and W. Schiefenhövel (eds.) Grandmotherhood: The evolution-
ary significance of the second half of female life. 295–317.
“Inkscape tutorial: tracing bitmaps | Inkscape.” n.d. Accessed November 29,
2018. https://inkscape.org/doc/tutorials/tracing/tutorial-tracing.html
Inside Nature’s Giants | PBS. n.d. Accessed November 29, 2018. www.pbs.org
/show/inside-natures-giants/
Jablonski, D. 2008. “Species selection: Theory and data.” Annual Review of
Ecology, Evolution, and Systematics 39(1): 501–24. https://doi.org/10.1146
/annurev.ecolsys.39.110707.173510
Jablonski, D., and G. Hunt. 2006. “Larval ecology, geographic range, and
species survivorship in Cretaceous mollusks: Organismic versus species-
level explanations.” The American Naturalist 168(4): 556–64. https://doi
.org/10.1086/507994
Jacob, F. 1977. Evolution and tinkering. Science 196(4295): 1161–66.
Kerr, B., and P. Godfrey-Smith. 2002. “Individualist and multi-level perspectives
on selection in structured populations.” Biology and Philosophy 17(4): 477–517.
Ketterson, E. D., and V. Nolan Jr. 1999. “Adaptation, exaptation, and constraint:
A hormonal perspective.” The American Naturalist 154 (S1): S4–25. https://
doi.org/10.1086/303280.
Kinsey, A. C., W. B. Pomeroy, C. E. Martin, and P. H. Gebhard. 1953. Sexual
behavior in the human female. Indiana University Press.
Komisaruk, B., C. Beyer-Flores, and B. Whipple. 2006. The science of orgasm.
Baltimore: John Hopkins University Press.
Komisaruk, B. R., N. Wise, E. Frangos, W. Liu, K. Allen, and S. Brody. 2011.
“Women’s clitoris, vagina, and cervix mapped on the sensory cortex: FMRI
evidence.” The Journal of Sexual Medicine 8(10): 2822–30. https://doi.org
/10.1111/j.1743-6109.2011.02388.x
Laland, K. N., J. Odling-Smee, and M. W. Feldman. 2000. “Niche construction,
biological evolution, and cultural change.” Behavioral and Brain Sciences
23(1): 131–46. https://doi.org/10.1017/S0140525X00002417.
Lemmon, W. B., and M. L. Allen. 1978. “Continual sexual receptivity in the
female chimpanzee (Pan troglodytes).” Folia Primatologica 30, no. 1:
80–88.
Levin, R. J. 2011. “Can the controversy about the putative role of the human
female orgasm in sperm transport be settled with our current physiological
88 References
knowledge of coitus?” The Journal of Sexual Medicine 8(6): 1566–78.

https://doi.org/10.1111/j.1743-6109.2010.02162.x.
Levin, R. J. 2014. “Should the clitoris become a vestigial organ by personal
psychological clitoridectomy? A critical examination of the literature.”
Journal of Womens Health, Issues and Care. https://doi.org/10.4172/2325-
9795.1000159
Levin, R. J. 2015. “Recreation and procreation: A critical view of sex in the human
female.” Clinical Anatomy 28(3): 339–54. https://doi.org/10.1002/ca.22495.
Levins, R. 1966. “The strategy of model building in population biology.”
American Scientist 54(4): 421–31.
Lewens, T. 2009. “Seven types of adaptationism.” Biology & Philosophy 24 (2):
161–82 https://doi.org/10.1007/s10539-008-9145-7.
Lewontin, R. C. 1978. “Adaptation.” Scientific American 239(3): 213–31.
Lewontin, R. C. 1983. “Gene, Organism and Environment.” In
Bendal, D. S. (ed.) Evolution from molecules to men. Cambridge
University Press.
Lewontin, R. C., and L. C. Dunn. 1960. “The evolutionary dynamics of
a polymorphism in the house mouse.” Genetics 45(6): 705–22.
Li, D., and R. O’Loughlin. Manuscript. “Tractability assumptions, holism, and
model robustness.” Submitted.
Linde-Medina, M. 2011. “Adaptation or exaptation? The case of the human
hand.” Journal of Biosciences 36(4): 575–85. https://doi.org/10.1007
/s12038-011-9102-5
Linquist, S. P. 2006. “Sometimes an orgasm is just an orgasm.” Metascience 15
(2): 411–19.
Lloyd, E. A. 1983. “The nature of Darwin’s support for the theory of natural
selection.” Philosophy of Science 50 (1): 112–29. https://doi.org/10.1086/289093
Lloyd, E. A. 1988/1994. The structure and confirmation of evolutionary theory.
Princeton University Press.
Lloyd, E. A. 2001. “Units and levels of selection: An anatomy of the units of
selection debates.” In Rama S., C. B. Krimbas, J. Beatty, and D. B. Paul
(eds.). Thinking about evolution: Historical, philosophical, and political
perspectives (2): 267–91. Cambridge University Press.
Lloyd, E. A. 2005a. The case of the female orgasm: Bias in the science of
evolution. Cambridge, MA: Harvard University Press.
Lloyd, E. A. 2005b. “Why the gene will not return.” Philosophy of Science
72(2). 287–310.
Lloyd, E. A. 2013. “Stephen J. Gould and adaptation: San Marco 33 years later.”
In Stephen J. Gould: The Scientific Legacy. Springer, Milano. 21–35
References 89
Lloyd, E. A. 2015a. “Adaptationism and the logic of research questions: How to

think clearly about evolutionary causes.” Biological Theory 10(4): 343–62.
https://doi.org/10.1007/s13752-015-0214-2.
Lloyd, E. A. 2015b. “Model robustness as a confirmatory virtue: The case of
climate science.” Studies in History and Philosophy of Science Part A 49:
58–68.
Lloyd, E. A. 2017. “Units and levels of selection,” Stanford Encyclopedia of
Philosophy. www.plato.stanford.edu/entries/selection-units/
Lloyd, E. A., and S. J. Gould. 1993. “Species selection on variability.”
Proceedings of the National Academy of Sciences 90(2): 595–99. https://doi
.org/10.1073/pnas.90.2.595
Lloyd, E. A., and S. J. Gould. 2017. “Exaptation revisited: Changes imposed by
evolutionary psychologists and behavioral biologists.” Biological Theory
12(1): 50–65. https://doi.org/10.1007/s13752-016-0258-y
Lloyd, E. A., R. C. Lewontin, and M. W. Feldman. 2008. “The generational
cycle of state spaces and adequate genetical representation.” Philosophy of
Science 75(2), 140–56.
Lloyd, E. A., and M. J. Wade. 2019. “Criteria for holobionts from community
genetics.” Biological Theory 14(3): 151–70. 10.1007/s13752-019–00322-w
Lloyd, E. A., D. S. Wilson, and E. Sober. 2011. “Evolutionary mismatch and
what to do about it.” The Evolution Institute (blog). November 13, 2012.
https://evolution-institute.org/evolutionary-mismatch-and-what-to-do-about
-it/
Losos, J. B. 2011. “Seeing the forest for the trees: The limitations of phyloge-
nies in comparative biology.” The American Naturalist 177(6): 709–27.
https://doi.org/10.1086/660020
Love, A. C. 2003. “Evolutionary morphology, innovation, and the synthesis of
evolutionary and developmental biology.” Biology and Philosophy 18(2):
309–45.
Love, A. C. 2006. “Evolutionary morphology and evo-devo: Hierarchy and
novelty.” Theory in Biosciences 124(3): 317–33.
Marshall Cavendish Corporation. 2010. Mammal anatomy: An illustrated
guide. Illustrated edition. New York: Cavendish Square.
Martins, E. P. 2000. “Adaptation and the Comparative Method.” Trends in
Ecology & Evolution 15(7): 296–99. https://doi.org/10.1016/S0169-
5347(00)01880-2.
Masters, W. H. and V. E. Johnson. 1965. “The sexual response of the human
female.” In Money, J. (ed.). Sex Research: New Developments. 53–112.
New York: Holt, Rinehart, and Winston.
90 References
Masters, W. H. and V. E. Johnson. 1966. The human sexual response. Boston:

Little, Brown.
Maynard Smith, J. 1978. “Models in ecology.” CUP Archive.
Maynard Smith, J. 1993. The theory of evolution. Cambridge University
Press.
Mayr, E. 1983. “How to carry out the adaptationist program?” The American
Naturalist 121(3): 324–34. https://doi.org/10.1086/284064
Medeyko, V. 1986. The Collins Encyclopedia of Animal Evolution. Berry, R. J.
and A. Hallam (eds.). London: Collins.
Millstein, R. L. 2008. “Distinguishing drift and selection empirically: ‘The
great snail debate’ of the 1950s.” Journal of the History of Biology 41(2):
339–67. https://doi.org/10.1007/s10739-007-9145-5.
Muller, G. B., & Wagner, G. P. 1991. “Novelty in evolution: restructuring the
concept.” Annual Review of Ecology and Systematics 22(1): 229–56.
Murphy, C. G. 1998. “Interaction-independent sexual election and the mechan-
isms of sexual selection.” Evolution 52 (1): 8–18. https://doi.org/10.1111/j
.1558-5646.1998.tb05133.x
Newman, S. A. 1988. “Lineage and pattern in the developing vertebrate limb.”
Trends in Genetics 4 (12): 329–32.
Newman, S. A., and R. Bhat. 2008. “Dynamical patterning modules:
Physico-genetic determinants of morphological development and
evolution.” Physical Biology 5 (1): 015008. https://doi.org/10.1088/1478-
3975/5/1/015008
Newman, S. A., and R. Bhat. 2011. “Lamarck’s dangerous idea.” In Jablonka E.
and S. B. Gissis (eds.), Transformations of Lamarckism: From subtle fluids to
molecular biology. 157–70. Cambridge, Massachusetts Institute of
Technology Press.
Nijhout, F. H. 1991. The development and evolution of butterfly wing patterns.
Smithsonian Institution Scholarly Press.
Oakley, S. H., C. M. Vaccaro, C. C. Crisp, M. V. Estanol, A. N. Fellner,
S. D. Kleeman, and R. N. Pauls. 2014. “Clitoral size and location in relation
to sexual function using pelvic MRI.” The Journal of Sexual Medicine 11(4):
1013–22. https://doi.org/10.1111/jsm.12450.
Odenbaugh, J. 2018. “Emotions.” Ch. 4 Manuscript.
Odling-Smee, F. J., K. N. Laland, and M. W. Feldman. 2003. Niche construc-
tion: The neglected process in evolution. Princeton University Press.
Orzack, S. H., and E. Sober. 2001. Adaptationism and optimality. Cambridge
University Press.
Pavličev, M., A. M. Zupan, A. Barry, S. Walters, K. M. Milano, H. J. Kliman,
and G. P. Wagner. 2019. “An experimental test of the ovulatory homolog
References 91
model of female orgasm.” Proceedings of the National Academy of Sciences

116(41). 20267–73.
Pavličev, M., and G. P. Wagner. 2016. “The evolutionary origin of female
orgasm.” Journal of Experimental Zoology Part B: Molecular and
Developmental Evolution 326(6): 326–37.
Pinker, S. 1999. “How the mind works.” Annals of the New York Academy of
Sciences 882: 119–27.
Puts D. A., K. Dawood, and L. L. M. Welling. 2012a. “Why women have orgasms:
An evolutionary analysis.” Archives of Sexual Behavior 41 (5): 1127–43.
Puts, D. A., L. M. Welling, R. P. Burriss, and K. Dawood. 2012b. “Men’s
masculinity and attractiveness predict their female partners’ reported orgasm
frequency and timing.” Evolution and Human Behavior 33(1): 1–9. https://
doi.org/10.1016/j.evolhumbehav.2011.03.003.
Raff, R. A. 1996. The shape of life: Genes, development and the evolution of
animal form. University of Chicago Press.
Raff, R. A., and E. C. Raff. 2009. “Evolution in the light of embryos: Seeking
the origins of novelties in ontogeny.” In M. D. Laubichler and J. Maienschein
(eds.) Form and function in developmental evolutions. 83–111. Cambridge
University Press.
Reeve, H. K., and P. W. Sherman. 1993. “Adaptation and the goals of evolu-
tionary research.” The Quarterly Review of Biology 68(1): 1–32. https://doi
.org/10.1086/417909
Reznick, D., and J. Travis 1996. “The empirical study of adaptation in natural
populations.” In Rose, M. R., and G. V. Lauder (eds.), Adaptation. 243–89,
Academic Press.
Rose, M. R., and V. Lauder. 1996. Adaptation. Academic Press. https://aca
demic.oup.com/sysbio/article/47/3/538/1703769.
Russell, B. 1919. Introduction to mathematical philosophy. McMillan.
Sagan [Margulis], L. 1967. “On the origin of mitosing cells.” Journal of
Theoretical Biology 14 (3): 225-IN6. https://doi.org/10.1016/0022-
5193(67)90079-3
Sansom, R. 2003. “Constraining the adaptationism debate.” Biology and
Philosophy 18 (4): 493–512. https://doi.org/10.1023/A:1025581622161
Schmitt, D. P., and J. J. Pilcher. 2004. “Evaluating evidence of psychological
adaptation: How do we know one when we see one?” Psychological Science
15(10): 643–49. https://doi.org/10.1111/j.0956-7976.2004.00734.x
Seger, J, and J. W. Stubblefield. 1996. “Optimization and adaptation.” In
Rose, M. R., and G. V. Lauder (eds.) Adaptation. 93–102. Academic Press.
Sherman, P. W. 1989. “The clitoris debate and the levels of analysis.” Animal
Behaviour 37(4): 697–98. https://doi.org/10.1016/0003-3472(89)90052-3.
92 References
Shpak, M., and G. P. Wagner. 2000. “Asymmetry of configuration space

induced by unequal crossover: implications for a mathematical theory of
evolutionary innovation.” Artificial Life 6(1): 25–43. https://doi.org/10.1162
/106454600568302.
Sinervo, Barry, and A. L. Basolo. 1996. “Testing adaptation using phenotypic
manipulations.” In Rose, M. R., and G. V. Lauder (eds.) Adaptation.
149–185.
Smith, D. 2005. “A critic takes on the logic of female orgasm.” The New York
Times, May 17, 2005, sec. Science Times. www.nytimes.com/2005/05/17/
science/a-critic-takes-on-the-logic-of-female-orgasm.html.
Smith, M. J. 1978. “Optimization theory in evolution.” Annual Review of
Ecology and Systematics 9:31–56.
Song, N., A. Lin, and X. Zhao. 2018. “Insight into higher-level phylogeny of
Neuropterida: Evidence from secondary structures of mitochondrial rRNA
genes and mitogenomic data.” PLOS ONE 13 (1): e0191826. doi:10.1371/
journal.pone.0191826. ISSN 1932–6203.
Sterelny, K., and P. Kitcher. 1988. “The return of the gene.” The Journal of
Philosophy. 85(7): 339–361.
Suárez, J., and V. Triviño. 2020. “What is a hologenomic adaptation? Emergent
individuality and inter-identity in multispecies systems.” Frontiers in
Psychology. 11.
Sunquist, F. 2006. “Malaysian mystery leopards.” National Wildlife. www
.nwf.org/en/Magazines/National-Wildlife/2007/Malasian-Mystery.
Symons, D. 1979. The evolution of human sexuality. Oxford University Press.
Symons, D. 1990. “Adaptiveness and adaptation.” Ethology and Sociobiology
11(4): 427–44. https://doi.org/10.1016/0162-3095(90)90019-3.
Thornhill, R. 1990. “The study of adaptation.” In Bekoff, M., and D. Jamieson
(eds.) Readings in Animal Cognition. 31–62. Massachusetts Institute of
Technology Press.
Tooby, J., and L. Cosmides. 1997. “Letter to the editor of the New York Review of
Books on Stephen Jay Gould’s ‘Darwinian fundamentalism.’” New York Review
of Books, June 26, 1997. http://cogweb.ucla.edu/Debate/CEP_Gould.html.
Vaccaro, C. M. 2015. “The use of magnetic resonance imaging for studying
female sexual function: A review.” Clinical Anatomy 28 (3): 324–30. https://
doi.org/10.1002/ca.22531
Van Fraassen, B. C. 1977. “The pragmatics of explanation.” American
Philosophical Quarterly 14 (2): 143–50.
Wade, M. J. 1978. “A critical review of the models of group selection.” The
Quarterly Review of Biology 53 (2): 101–14. https://doi.org/10.1086/410450
References 93
Wade, M. J. 2016. Adaptation in metapopulations: How interaction changes

evolution. University of Chicago Press.
Wagner, G. P. 2015. “Evolutionary innovations and novelties: Let us get down
to business!” Zoologischer Anzeiger-A Journal of Comparative Zoology 256:
75–81.
Wagner, G. P. 2000. “What is the promise of developmental evolution? Part i:
Why is developmental biology necessary to explain evolutionary
innovations?” Journal of Experimental Zoology 288 (2): 95–98.
Wake, D. B. 1991. “Homoplasy: The result of natural selection, or evidence of
design limitations?” The American Naturalist 138 (3): 543–67. https://doi
.org/10.1086/285234
Wake, D. B. 2009. “What salamanders have taught us about evolution.” Annual
Review of Ecology, Evolution, and Systematics 40 (1): 333–52. https://doi.org
/10.1146/annurev.ecolsys.39.110707.173552
Wallen, K., and E. A. Lloyd. 2011. “Female sexual arousal: Genital anatomy
and orgasm in intercourse.” Hormones and Behavior, Special Issue on
Research on Sexual Arousal 59(5): 780–92. https://doi.org/10.1016/j
.yhbeh.2010.12.004.
Wallen, K., E. A. Lloyd, and P. Z. Myers. 2012. “Zietsch & Santtila’s study is
not evidence against the by-product theory of female orgasm.” Animal
Behaviour 84(5): e1–e4.
Weisberg, M. 2006. “Robustness analysis.” Philosophy of Science 73(5):
730–42.
Wheatley, J. R., and D. A. Puts. 2015. “Evolutionary science of female orgasm.”
In Shackelford, T. K., and R. D. Hansen (eds.) The evolution of sexuality.
Springer International Publishing. 123–48. https://doi.org/10.1007/978-
3-319-09384-0_7
Wikelski, M., V. Carrillo, and F. Trillmich. 1997. “Energy limits to body size
in a grazing reptile, the Galapagos marine iguana.” Ecology 78 (7):
2204–17.
Wikelski, M., and C. Thom. 2000. “Marine iguanas shrink to survive El Niño.”
Nature 403 (6765): 37–38. https://doi.org/10.1038/47396
Wikimedia Commons contributors. 2018. “File:GiraffaRecurrRu.Svg.” https://
Commons.Wikimedia.Org. November 29, 2018. https://commons.wikimedia
.org/w/index.php?title=File:GiraffaRecurrRu.svg&oldid=278005938
Williams, G. C. 1966. Adaptation and natural selection. Princeton University
Press.
Woodward, J. 2006. “Some varieties of robustness.” Journal of Economic
Methodology 13(2): 219–40.
94 References
Wright, L. 1973. “Functions.” The Philosophical Review 82(2): 139–68.

doi:10.2307/2183766
Wright, S. 1931. “Evolution in Mendelian populations.” Genetics 16 (2):
97–159.
Zietsch, B. P., and P. Santtila. 2011. “Genetic analysis of orgasmic function in
twins and siblings does not support the by-product theory of female orgasm.”
Animal Behaviour 82 (5): 1097–1101. https://doi.org/10.1016/j
.anbehav.2011.08.002
Zietsch, B. P., and P. Santtila. 2013. “No direct relationship between human
female orgasm rate and number of offspring.” Animal Behaviour 86 (2):
253–55. https://doi.org/10.1016/j.anbehav.2013.05.011
Zuk, M. 2006. “The case of the female orgasm (review).” Perspectives in
Biology and Medicine 49 (2): 294–98.
Acknowledgments
Thank you to Arnold and Maxine Tanis for their support of my research over
many years. I owe thanks to many biologists and philosophers for discussion
about the topic of this book over many years, including especially the follow-
ing: The Biology Studies Reading Group at IU, Colin Allen, Linnda Caporael,
Janet Collett, Michael Dietrich, Stephen Downes, Marcus Feldman, Justin
Garcia, Stephen Jay Gould, Jim Griesemer, Chris Haufe, David Hull, Ryan
Ketcham, Roy Levin, Richard Lewontin, Daniel Lindquist, Alan Love,
Eduoard Machery, Gordon McOuat, Roberta Millstein, Elizabeth and Rudy
Raff, Michael Ruse, Elliott Sober, Javier Suarez, Donald Symons, Michael
Wade, Michael Weisberg, David Sloan Wilson, Stuart Newman, and two
anonymous referees for Biological Theory. Please forgive me, those I have
not mentioned due to my faulty memory!
Grant Ramsey
KU Leuven
Grant Ramsey is a BOFZAP research professor at the Institute of Philosophy, KU Leuven,
Belgium. His work centers on philosophical problems at the foundation of evolutionary
biology. He has been awarded the Popper Prize twice for his work in this area. He also
publishes in the philosophy of animal behavior, human nature and the moral emotions. He
runs the Ramsey Lab (theramseylab.org), a highly collaborative research group focused on
issues in the philosophy of the life sciences.
Michael Ruse
Florida State University
Michael Ruse is the Lucyle T. Werkmeister Professor of Philosophy and the Director of the
Program in the History and Philosophy of Science at Florida State University. He is Professor
Emeritus at the University of Guelph, in Ontario, Canada. He is a former Guggenheim fellow
and Gifford lecturer. He is the author or editor of over sixty books, most recently Darwinism
as Religion: What Literature Tells Us about Evolution; On Purpose; The Problem of War:
Darwinism, Christianity, and Their Battle to Understand Human Conflict; and A Meaning to
Life.
About the Series

This Cambridge Elements series provides concise and structured introductions to all of the
central topics in the philosophy of biology. Contributors to the series are cutting-edge
researchers who offer balanced, comprehensive coverage of multiple perspectives, while
also developing new ideas and arguments from a unique viewpoint.
Philosophy of Biology
Elements in the Series

The Biology of Art
Richard A. Richards
The Darwinian Revolution
Michael Ruse
Ecological Models
Jay Odenbaugh
Mechanisms in Molecular Biology
Tudor M. Baetu
The Role of Mathematics in Evolutionary Theory
Jun Otsuka
Paleoaesthetics and the Practice of Paleontology
Derek D. Turner
Philosophy of Immunology
Thomas Pradeu
The Challenge of Evolution to Religion
Johan De Smedt and Helen De Cruz
The Missing Two-Thirds of Evolutionary Theory
Robert N. Brandon and Daniel W. McShea
Games in the Philosophy of Biology
Cailin O’Connor
How to Study Animal Minds
Kristin Andrews
Inheritance Systems and the Extended Evolutionary Synthesis
Eva Jablonka and Marion J. Lamb
Reduction and Mechanism
Alex Rosenberg
Model Organisms
Rachel A. Ankeny and Sabina Leonelli
Comparative Thinking in Biology
Adrian Currie
Social Darwinism
Jeffrey O’Connell and Michael Ruse
Adaptation
Elisabeth A. Lloyd
A full series listing is available at: www.cambridge.org/EPBY

Adaptation

Uploaded by

Copyright:

Available Formats

Adaptation

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Adaptation

Uploaded by

Copyright:

Available Formats

Lloyd

Natural selection causes adaptation, the fit between an

Cover image: Ascidiae from Kunstformen der Natur (1904)

Cambridge University Press is part of the University of Cambridge.

Elements in the Philosophy of Biology

DOI: 10.1017/ 9781108634953

Abstract: Natural selection causes adaptation, the ﬁt between an

Keywords: evolutionary adaptation, evolutionary causes, development and

© Elisabeth A. Lloyd 2021

1 What Are Adaptations? 1

3 Adaptationism and the Logic of Research Questions 34

4 Case Studies Showing the Inadequacy of Methodological

1 What Are Adaptations?

1.2 Evolutionary Models

forms of moth in this case: There is no engineering or cumulative adaptation

Table 1.1 Deﬁnitions2

BOX 1.1 NATURAL SELECTION MODEL OUTLINE

increases ﬁtness, as well as a description of a selection scenario that describes

Understanding this involves reconstructing the ancestors of the current popu-

When these experiments are done, it may be possible to determine which

Etiological approaches to function look to a causal-historical process of

are identiﬁed with their causal contributions to broader capacities of the

1.2 Conﬁrming Evolutionary Models

There are several basic types of supporting evidence and conﬁrmation:

Cren/Riv (Days) Eleo/R-M (Days) Cren/Riv (mg) Eleo/R-M (mg)

Figure 1.2 Decrease of age at sexual maturity depending on predator (Reznick

Figure 1.3 Selection regimes: stabilizing vs. directional selection5

1.2.2 Independent Support for Aspects of the Model

As exciting as it is to have selective model predictions be supported by evidence

1.2.3 Variety of Evidence

A third distinct type of evidence for selection models is variety of evidence, of

BOX 1.2 FILLED-IN NATURAL SELECTION MODEL

Population [guppy population]

When an evolutionary model demonstrates compatibility with a very broad

Variety of Independent Support for Aspects of the Model

BOX 1.3 VARIETY OF ROBUST EVIDENCE

- More frequent reproduction

Robustness: Variety of Robust Evidence

1.2.4 Totality of Types of Evidence Together

BOX 1.4 TYPES OF SUPPORTING EVIDENCE FOR SELECTION MODELS

4. Robustness: Variety of robust evidence

adaptation properly in evolution includes not only evidence of a contribution to

2.4 Phyletic Constraint

Figure 2.1 Scheme of path of the recurrent laryngeal nerve in Giraffe

2.5 Developmental Constraints and the Origin of Evolutionary

DEFINITION: A morphological novelty is a structure that is neither homolo-

The sutures in the skulls of young mammals have been advanced as

Figure 2.3 Independent four-toed lineages in the salamander family

evolutionary innovation, we need a new coordinate system – a new set of

after the emergence of an evolutionary innovation, we need a new coordinate

In other words, Wagner emphasizes the importance of including the evolution of

2.6 Genetic Linkage

By ﬁnding recombination frequencies for the various gene pairs, we can

2.8 Cultural Coevolution Factors

represents a good example of gene-culture coevolution. There is systematic

2.9 Niche Construction

[N]iche construction modiﬁes one or more sources of natural selection

This feedback generated through niche construction constitutes the primary

2.10 Sexual Selection

Darwin deﬁned two major types of sexual section: