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BIOL2007 EVOLUTION OF SEX AND SEXUAL

SELECTION
EVOLUTIONARY QUESTIONS ABOUT SEX
Today:
A) The evolution of sex
1) What is the advantage of sex?
2) What is the optimal sex ratio?
B) Ev. of sexual dimorphism - sexual selection
3) Why are there "secondary sexual
characteristics"

OTHER interesting questions could be asked:
4) Why has meiosis evolved to share out
chromosomes?
5) Why are mitochondria and organelles NOT
shared equally?
6) Why are there only 2 sexes?
7) How does sex determination evolve?

See: BIOL2011 (Behavioural Ecology and Sociobiology)
and BIOL3012 (Sex, Genes and Evolution).

WHAT IS SEX?
Recombination all of life
Meiosis - eukaryotes only
Anisogamy - unequal gamete size - multicell
eukaryotes
Dioecy - Separate sexes - vs. hermaphrodites
and monoecy

These are complex energy-requiring traits
ADAPTATIONS.
Recombination seems to be a lowest common
denominator of all sex.

EVOLUTION OF SEX

Costs of sex
Recombination and sex is complicated, costly,
predation-prone (even if fun).
Two-fold cost of sex. Populations grow faster if pure
parthenogens. Suppose each female produces 2.4
progeny:
Generation Parthenogenetic Sexual

0 100 females 100 females (+ 100 males)

1 240 females 120 females (+ 120 males)

2 576 females 144 females (+ 144 males)

... and so on (but it works for any reprod. rate)
Males contribute little; males are useless! Parthenogens
outdo sexual females and increase in frequency.
Advantage not always twofold
If such strong disadvantages to dioecy,
must be some pretty hefty advantages.
Recombination is the primary feature of sex.
Advantages of sex must have something to do with
recombination.
Advantages of sex
a) recombination increases ev. rate
Muller: Recombination allows advantageous mutations
to combine in the same individuals.

Species compete, so a higher evolutionary rate can be
adaptive for a species.
May work against individual disadvantages for sex within
populations: so a form of group selection.
Asexual "cheats" might gain individual advantage and
spread to fixation within their own species, but cannot
spread to other species.
If other species have higher evolutionary rate, may
cause extinction of asexual species: one of the few
cases where people believe that group selection may
actually be operating.
Evidence: asexual species trapped on twigs in
phylogenies; do not produce many progeny species.
Asexual (clone) lineages, also often seem trapped in
some areas where they can compete.
Sexual forms are found in habitats where asexuals
cannot invade.
For example, many weeds of human cultivation are
asexuals, but sexual relatives live in more complex non-
cultivated environments. (e.g. dandelions)

b) Individual selection
Normally, evolutionists are often suspicious of group
selection explanations.
Some species: facultatively asexual, e.g. aphids, or
water fleas (Daphnia).
Sexuals persist in many lineages in competition with
asexuals. --> implies individual selection:
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Survival in a coevolutionary "arms race".
If the environment of offspring very different from that of
parent, parents adaptations may not be sufficient.
Sex as a lottery for producing at least some progeny
with reshuffled adaptations - a direct individual selection
advantage to parents in producing recombined offspring.
Other ideas. There are plenty, but we will leave that to
other courses.

EVOLUTION OF THE SEX RATIO
In dioecious organisms, sex ratio usually ~1:1.
Darwin puzzled, and eventually gave up, admitting that
the subject was too complicated!
RA Fisher: frequency-dependent selection.

1.0 (Conover & Voorhees, Science 1990; fish Menidia)

prop Low temperature
females

0.5
1 time (generations) 9


High temperature
0.0
Conover & Voorhees experiment accords with Fishers
frequency-dependent sex-ratio theory:
It isnt the ratio of of numbers of the sexes that matters,
but the ratio of investment.
Females should invest about their resources in male
production and female production.
EVOLUTION OF SEXUAL DIMORPHISM - SEXUAL
SELECTION
Darwin explained secondary sexual characteristics as
due to a struggle for genetic representation between
members of the same sex.
He contrasted sexual selection (struggle for mating
success) with natural selection (struggle for survival and
reproduction after mating).
Nowadays: sexual selection as a special form of natural
selection, but a very important one.
Why are males more extreme?
Most often, males are more flamboyant than females,
with horns, bright colours, or displays [SHOW SOME
EXAMPLES].
Why is it usually this way around? Darwin's view was
that males are more "passionate" than females , due to
the need for energetic males to seek out females. But
why do males seek females, rather than the other way
round?
Males:
cheap gametes
can produce lots
little parental investment
potentially father many offspring
Females:
expensive gametes
often show more parental care, at least as far as
nutrients in the egg
limited number of offspring than males
Males:
compete for access to females
more indiscriminate, less to lose
Females:
plenty of willing males around
worthwhile to be choosy, because number of
matings doesnt limit offspring number.

In Drosophila, females little extra benefit from fooling
around
males' fitnesses are roughly proportional to the number
of matings.

Greater struggle for matings among males males
under greater sexual selection. Females rarely benefit
much from more mates; males benefit from virtually
unlimited matings.

In elephant seals, > 90% males father no offspring; The
fittest male fathered 93. But> 50% females have one or
more offspring. Males have higher variance in offspring
number.
Quite likely that sexual selection may obtain increased
matings at the expense of reduced survival.
Darwin argued that sexual selection could outweigh
natural selection, and explain much conspicuous
coloration in the animal kingdom. Sexual selection can
antagonize natural selection for camouflage.
Darwin: two major types of sexual selection:
Intrasexual selection - male-male competition in
which males compete, often by fighting for females. And

Intersexual selection - sexual selection by female
choice, in which males compete for the favours of
females.
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Intrasexual selection - male-male competition
a) Selection for fighting ability
Relatively uncontroversial.
But not always appreciated, at least by laymen who
believe in balance of nature, that serious injury, even
death may result from fights between males.
(Not getting mated is genetic death!)
Examples:
Red deer males: harems of females, defend by
roaring, displaying, and finally fighting; injuries and death
may result.
Salmon: males fight to the death with enlarged
hooklike jaws, useless for feeding. All males die at the
end of season; so competition very severe.
Fig wasps: in some species, specialized males with
huge jaws hatch out and kill other males, before mating
with all the females in the fig.
b) Sperm competition
Male-male competition: after females mate multiply.
Here, sexual selection between sperm of rival males for
fertilization of eggs, often in the reproductive tract of
females.
In primates, males from species with more polyandry
have larger testes than males from monandrous
species.
Gorillas are monandrous, and have smaller testes than
human males!
(But chimps have bigger testes than us).
Sperm competition, like other forms of fighting, can have
nasty effects on the female too.
Tracey Chapman (UCL Biology) has shown this in
Drosophila. Mated females age faster than unmated
females, due male accessory gland proteins.

Intersexual selection - sexual selection via female
choice
Sexually dimorphic traits seem costly.
Costly display traits can evolve if females actively
choose males with more exaggerated traits.
Darwin: females have an "aesthetic sense", but few
believed him, perhaps understandably.
Wallace, believed most sexual dimorphism not costly;
instead due to display in male-male competition.
RA Fisher: theoretical analyses rehabilitated female
choice in the 1930s.
Today, an explosion of work showing females do indeed
choose, and that sexually selected traits are indeed
often costly.
For example: Anders Mllers barn swallows.
But why SHOULD females choose males with
exaggerated and costly traits?
Three major theories:

a) Sensory bias. A modern version of Darwins
hypothesis. Recognition requires a preference
exaggerated traits. Exaggeration a supernormal sign
stimulus for the natural male.
Pre-existing preferences: Physalaemus frog phylogeny
shows that an odd "chuck" sound has evolved in a
terminal branch of the genus.
Females of related spp. which lack the "chuck" still like
it. (Mike Ryan, University of Texas).
Sensory bias can explain some features of dimorphism
but additional ideas to explain why some traits are very
costly.

b) Direct benefits of female choice
Avoiding disease by mating with uninfected males.

c) Indirect benefits of female choice Indirect benefits
are passed on to the offspring via genetic contribution
from male.

i) sexy sons.
Mathematical models, by Russ Lande and Mark
Kirkpatrick (1980s): runaway models of sexual selection.
Imagine male trait evolution and female choice; females
can choose whatever they want;
males have a natural-selection optimum.

A line of neutral equilibrium (neither stable or unstable)
along which populations may drift.
Coevolution of male trait and female response;
Sometimes; evolves towards the line of neutral
equilibrium, whereupon evolution will stop.
In other cases evolution can angle away from the line of
neutral equilibrium; a runaway process of evolution.
The Kirkpatrick/Lande runaway involves linkage
disequilibrium between genes for male trait and genes
for female choice.
Females are selected to mate with extreme males; and
produce males that are themselves favoured, i.e. "sexy
sons".
Runaway eventually stops via natural selection;
alternatively, the population could go extinct because of
the extreme exaggeration. Like the ?Irish Elk.
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ii) "good genes hypothesis". Females choose males
with exaggerated, costly traits as "badges" which
indicate high fitness.
Here females are selecting exaggerated males because
all of their progeny will be fitter; they have "good genes".
Sickly development means it will be more difficult to
produce exaggerated traits.
The parasite hypothesis of Hamilton and Zuk. Male
bird and mammal displays often involve bare patches of
skin (e.g. baboons bottoms, wattles on cockerels).
Blood diseases, parasitism: changes the colour of blood
(e.g. diseases of chickens).
These displays are honest signals of health.
Hamilton & Zuk: sexually dimorphic species of birds tend
to suffer more from parasites.
Another variant of good genes idea is Zahavis
"handicap principle".
Non-costly male badges prone to cheating
Zahavi: only a very costly trait uncheatable
A costly "handicap" is selected, paradoxically, because it
guarantees "honest signalling".
Tests between ideas for the evolution of costly traits
None of the three ideas ruled out.
"Good genes" makes clear empirical predictions about
fitness of progeny.
Anders Mller: longer-tailed male barn swallows chosen
by females, but also fewer blood-sucking mites
Mite load heritable. However, females also directly
benefit, by avoiding infection, even before any indirect
advantage for offspring.
Non-adaptive "sexy sons" idea appealing, but difficult to
prove. Need to show that trait has no direct or future
"good genes" benefit. (Hard!)
Neutral line of equilibria seems inescapable.
Sexual (or natural) selection is competition, and may not
always give greater adaptation; selection can drive us
away from optimum.
Semantic problems with handicap principle: How can a
trait which is nonadaptive (i.e. costly) also be adaptive
(signal of high fitness)?
Anyway, though evolutionists havent yet resolved these
arguments, they are fun to think about.

Sexual selection in humans
Darwin: "The Descent of Man and Selection in Relation
to Sex". Sexual selection explained the extraordinary
racial differences in animals and humans.
Desmond Morris, Jared Diamond, evolutionary
psychologists: similar conclusions.
Human features like:
lips
hair colour, skin colour
breasts in females, beard in males
copulation when not in oestrus
weapons, war?
ornaments, jewellery?
music?
art?
... etc.
TAKE HOME POINTS
Evolution of sex:
The basis of sex is recombination.
Separate sexes may be costly
Separate sexes may exist because:
o group selection against asexuality
o offspring variability (individual selection)
Sex ratios stabilize near 1:1, a form of
frequency-dependent selection
Sexual selection for exaggerated male traits:
Male-male competition
o fighting
o sperm competition
Female choice
o sensory bias
o direct benefit to self or offspring
o indirect, inherited benefits
S sexy sons
S good genes
FURTHER READING
Douglas J. Futuyma. 2005. Evolution.
Ch 14: 329-339, Ch 17: 417-426.

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