Arboreality has allowed for the evolution of increased
longevity in mammals
Milena R. Shattuck and Scott A. Williams1
Department of Anthropology, University of Illinois, Urbana, IL 61801
Edited by Alan Walker, Pennsylvania State University, University Park, PA, and approved January 28, 2010 (received for review October 2, 2009)
senescence
| extrinsic mortality | terrestriality | marsupials |
S
primates
enescence, or aging, is an intrinsic biological phenomenon that
limits an organism’s maximum potential lifespan, even in the
absence of extrinsic sources of mortality such as predation, disease,
and environmental hazards. Its evolution is of particular interest in
life-history studies (1, 2), in part because it is not immediately clear
why senescence persists in the presence of natural selection, which
might be expected to eliminate it. The evolutionary theory of aging,
in its several, nonmutually exclusive forms (3–8), proposes that
senescence is the result of late-acting, deleterious mutations that
accumulate because of the diminishing effectiveness of selection
with increasing age. Extrinsic mortality is one major factor that
contributes to the accumulation of deleterious mutations by limiting
exposure of these late-acting mutations to selection; thus, the evolutionary theory of aging predicts that extrinsic mortality will be a
principal determinate of the rate of senescence in age-structured
populations (9). This theory predicts that populations experiencing
high extrinsic mortality rates will accumulate more deleterious
mutations, evolve earlier senescence and reproduction, low somatic
maintenance, and shorter maximal lifespans. Conversely, populations subject to low extrinsic mortality rates will eliminate lateacting deleterious mutations more effectively and evolve delayed
senescence, late fecundity, durable somas, and greater longevities.
These relationships have been demonstrated in laboratory (10–12),
wild (13–15), and simulation (16) studies.
In the wild, flying birds and bats experience lower rates of extrinsic
mortality (17) and greater longevity (18–23) than their nonvolant
relatives, presumably because of decreased predation. Although
www.pnas.org/cgi/doi/10.1073/pnas.0911439107
other factors such as hibernation and reproductive rate have been
shown to play a role in bat longevity (22), these factors are accordant
with evolutionary theory of aging, and it is clear that the exceptional
longevity of Chiroptera as a whole is the result of flight. In addition to
flying birds and mammals, gliding mammals are longer-lived than
nonvolant, nongliding mammals (21, 23). As with flight and gliding
behavior, arboreality may act to lower extrinsic mortality rates and
increase longevity by providing a relatively protected environment
with reduced exposure to predation, disease, and environmental
hazards. Indeed, Darwin himself (ref. 24, p. 169) identified an
association between arboreality and extrinsic mortality, recognizing
the “power of quickly climbing trees, so as to escape from enemies.”
Furthermore, several researchers have suggested that primates are
long-lived among mammals at least in part because they are largely
arboreal (25, 26). If so, then we might expect arboreal mammals in
general to possess greater longevities than their terrestrial counterparts. Using analysis of covariance (ANCOVA) and an analysis of
phylogenetically independent contrasts (PIC), we test this hypothesis by comparing longevity records for arboreal and terrestrial
mammals in a molecular phylogenetic context (Fig. 1 and Fig. S1).
Results and Discussion
Overall, in agreement with previous studies (27, 28), body mass
accounts for 60% of the variance in maximal lifespan in nonvolant,
nonaquatic mammals. Longevity, like many life-history traits, is
negatively allometric, so that lifespan increases at between onefourth and one-third the rate of body mass (Fig. 2). An initial
analysis on the entire dataset indicates that the slope for semiarboreal species is significantly different from the arboreal and
terrestrial slopes. A separate analysis of Eutheria alone results in
common slopes for all three groups (see below; Table 1), suggesting
that the departure of the semiarboreal slope results from the
influence of marsupials. Because of this result, semiarboreal species
were removed for analysis on the overall dataset, and an ANCOVA
was conducted on the remaining habitat groups (arboreal and terrestrial). This analysis demonstrates that, at common body sizes,
arboreal mammals are characterized by greater longevities than
terrestrial mammals (P < 0.001) (Table 1 and Fig. 2). Results of the
PIC analysis on the mammalian dataset also are significant (P <
0.001), indicating the effect of habitat type on longevity remains
even when the effects of phylogeny are removed.
Results of subsequent ANCOVA are listed in Table 1. In 8 of the
10 subclades included in the analysis, arboreal mammals are characterized by greater longevities than terrestrial mammals (Table 1).
Semiarboreal eutherian mammals are either intermediately longlived or are not significantly different from one or the other habitat
type (Table 1 and Fig. 3). Results for two subclades, Metatheria
(marsupials) and Euarchonta (primates and their close relatives),
Author contributions: M.R.S. and S.A.W. designed research, performed research, analyzed
data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed. E-mail: sawill@gmail.com.
This article contains supporting information online at www.pnas.org/cgi/content/full/
0911439107/DCSupplemental.
PNAS | March 9, 2010 | vol. 107 | no. 10 | 4635–4639
EVOLUTION
The evolutionary theory of aging predicts that species will experience delayed senescence and increased longevity when rates of
extrinsic mortality are reduced. It has long been recognized that birds
and bats are characterized by lower rates of extrinsic mortality and
greater longevities than nonvolant endotherms, presumably because flight reduces exposure to terrestrial predators, disease, and
environmental hazards. Like flight, arboreality may act to reduce
extrinsic mortality, delay senescence, and increase longevity and has
been suggested as an explanation for the long lifespans of primates.
However, this hypothesis has yet to be tested in mammals in general.
We analyze a large dataset of mammalian longevity records to test
whether arboreal mammals are characterized by greater longevities
than terrestrial mammals. Here, we show that arboreal mammals are
longer lived than terrestrial mammals at common body sizes, independent of phylogeny. Subclade analyses demonstrate that this
trend holds true in nearly every mammalian subgroup, with two
notable exceptions—metatherians (marsupials) and euarchontans
(primates and their close relatives). These subgroups are unique in
that each has experienced a long and persistent arboreal evolutionary history, with subsequent transitions to terrestriality occurring
multiple times within each group. In all other clades examined, terrestriality appears to be the primitive condition, and species that
become arboreal tend to experience increased longevity, often independently in multiple lineages within each clade. Adoption of an
arboreal lifestyle may have allowed for increased longevity in these
lineages and in primates in general. Overall, these results confirm the
fundamental predictions of the evolutionary theory of aging.
Fig. 1. Molecular phylogeny of Mammalia. Prototheria: monotremes. Metatheria: marsupials. Afrotheria: aardvark, tenrecs, elephant shrews, hyraxes,
manatees, dugongs, elephants. Xenarthra: sloths, anteaters, armadillos.
Euarchonta: tree shrews, colugos, primates. Glires: rodents, rabbits. Eulipotyphla: moles, hedgehogs, shrews. Cetartiodactyla: bovids, cervids, suiforms,
camelids, hippopotamids, cetaceans. Chiroptera: bats. Ferae: Pholidota (manids)
and Carnivora (canids, ursids, musteloids, pinnipeds, felids, viverrids, herpestids,
hyaenids). Perissodactyla: horses, tapirs, rhinos.
differ from the overall results. Within Metatheria, although arboreal
and terrestrial marsupials are not significantly different from each
other, both are significantly longer-lived than semiarboreal taxa
(Table 1). Our results therefore confirm a previous finding that
arboreality is not associated with increased longevity in marsupials
(29). In Euarchonta, our analyses did not reveal significant differences between any of the habitat types (Table 1). However, taken
together, the overall results demonstrate that there is a general,
significant relationship between habitat type and longevity in
mammals. That is, arboreal mammals have evolved greater longevities than terrestrial mammals, and semiarboreal mammals tend
to fall intermediately between these two groups. Even in the most
specific clade we analyzed, the superfamily Sciuroidea, arboreal
squirrels are longer-lived than terrestrial squirrels at common body
sizes (P < 0.001; Fig. 3).
Previous authors have suggested that primates are particularly
long-lived among mammals, in part because they are largely
arboreal (25, 26). However, among both euarchontans and
marsupials, arboreal species do not possess greater longevities
than terrestrial species. Arboreality is the primitive condition for
Fig. 2. Maximal lifespan plotted against body mass for 776 mammals in log
space. The solid line is the least squares regression for terrestrial mammals;
the dashed line is the least squares regression for arboreal mammals. The
slopes for these regression lines are common, and the intercepts are significantly different (P < 0.001). OLS regression for arboreal mammals: y =
0.245x + 1.64, r2 = 0.499, P < 0.001. OLS regression for terrestrial mammals:
y = 0.222x + 1.39, r2 = 0.756, P < 0.001.
primates, initially evolved in an ancestral euarchontan (30–35).
Marsupials also probably are primitively arboreal (34, 36–38),
with subsequent and repeated events of terrestriality (38). In
contrast, many other eutherian orders and placental mammals in
general are likely characterized by terrestrial evolutionary histories, with subsequent events of arboreality derived multiple
times in these lineages (34, 39). (See ref. 34 and sources therein
for a recent and thorough review of this topic.) The nature of
these dichotomies may play out in the evolution of longevity. We
propose that the lack of significant differences between arboreal
and terrestrial euarchontans, and possibly marsupials, may be the
result in part of the long history and persistence of arboreality in
their evolutionary histories (30–38). Unlike euarchontans, however, marsupials are not characterized by increased longevity in
general (Fig. 4). Compared with marsupials, the extremely high
degree of arboreality throughout the evolution of Euarchonta,
Table 1. Clades, sample sizes, and significance
Significance (P value)*
Clade
Mammalia
Metatheria
Eutheria
Atlantogenata
Boreoeutheria
Laurasiatheria
Ferae
Euarchontoglires
Euarchonta
Glires
Sciuroidea
Sample size total A:S:T
776
081
693
030
663
281
122
382
154
228
051
(189:118:469)
(022:011:048)
(167:107:419)
(003:006:021)
(164:101:398)
(015:035:231)
(015:035:072)
(149:066:167)
(119:031:004)
(030:035:163)
(019:014:018)
Arboreal vs. terrestrial
Arboreal vs. semiarboreal
Terrestrial vs. semiarboreal
<0.001
NS
<0.001
0.030
<0.001
<0.001
<0.001
<0.001
NS
<0.001
<0.001
N/A
0.003
<0.001
NS
<0.001
0.050
NS
N/A
NS
0.012
0.032
N/A
0.015
<0.001
NS
<0.001
<0.001
0.002
N/A
NS
0.050
NS
*Bold P values indicate that the intercept for the more arboreal taxon is significantly greater than the intercept for the more terrestrial taxon at the α = 0.05 level.
Italicized P values indicate that the intercept for the more terrestrial taxon is significantly greater than the intercept for the more arboreal taxon. A:S:T, arboreal:
semiarboreal:terrestrial, N/A, assumptions of ANCOVA are not met (i.e., slopes were not found to be common); NS, nonsignificant P value (> 0.05).
4636 | www.pnas.org/cgi/doi/10.1073/pnas.0911439107
Shattuck and Williams
and specifically within primates, may explain this discrepancy. A
highly arboreal evolutionary history may have allowed increased
longevity in all primates.
In addition to a long arboreal evolutionary history, it has been
suggested that terrestrial primates may not experience increased
extrinsic mortality because they have evolved physiological, social,
and behavioral defenses against predation (40, 41). First, grounddwelling primates have increased body size upon transitioning to a
terrestrial lifestyle. Unlike other groups of mammals (e.g., carnivores; ref. 42), body mass is significantly correlated with habitat type
in primates (43). It is likely that the larger body size of terrestrial
primates decreases their susceptibility to predation, thus lowering
the risk of spending time on the ground (1, 40, 41, 43, 44). Predation
Fig. 4. Maximal lifespan plotted against body mass for Metatheria and
Euarchonta in log space. In both groups, arboreal and terrestrial intercepts
are not significantly different from each other (P > 0.05). The solid line is the
least squares regression for Mammalia, demonstrating the proximity of
marsupials (n = 81) and euarchontans (n = 154) to this line. OLS regression for
Mammalia: y = 0.225x + 1.49, r2 = 0.594, P < 0.001.
Shattuck and Williams
on small-bodied, arboreal primates by birds of prey and arboreal
carnivores and leopard predation on primates both on the ground
and in the trees may render arboreal and terrestrial primates equally
susceptible to predation (40, 41). Second, primates are highly social,
and the advantages of group living provide social defenses such as
large group size, vigilance, and alarm calls (40). Terrestrial primates
live in larger social groups than arboreal primates (40, 41, 43, 44),
thus supporting this hypothesis. Humans, the most terrestrial of all
primates, have reduced extrinsic mortality and increased longevity
resulting from the obvious advantages provided by sociality
and culture.
Similar arguments may be made for some marsupial species.
Terrestrial marsupials that occupy open habitats are generally
large and capable of fast speed (e.g., macropodids). In addition,
they live in large social groups and demonstrate vigilance
behavior, contrasting with the lack sociality of marsupials in
general (45–47). These factors might contribute to decreased
predation risks associated with terrestriality and explain the lack
of significant difference in longevity between arboreal and terrestrial marsupial species. However, as noted previously, marsupials are not long-lived in general, regardless of habitat type. This
observation suggests that other confounding factors, such as
development, brain size, or various aspects of physiology may
significantly influence longevity in these species. We therefore are
more cautious in our interpretation of marsupial longevity.
Many evolutionary transitions to arboreality among mammals
have resulted in increased longevity, demonstrated by longerlived arboreal taxa in the majority of mammalian clades. As with
flight and gliding behavior, arboreality appears to have reduced
extrinsic mortality and allowed increased longevity in many
groups of placental mammals. Future studies should test this
hypothesis by comparing mortality rates among closely related
species that occupy different habitats. The highly arboreal evolutionary history of Euarchonta, and especially primates, may
have allowed increased longevity in the group as a whole. This
hypothesis will require further testing, as will other mechanisms
that might influence extrinsic mortality, and therefore longevity,
including body size, sociality, behavioral and morphological
defenses, and adaptation to other habitat types (e.g., fossoriality). In summary, results of this study support the hypothesis
that primates and other arboreal mammals are characterized by
greater longevities than terrestrial mammals and confirm the
fundamental predictions of the evolutionary theory of aging.
PNAS | March 9, 2010 | vol. 107 | no. 10 | 4637
EVOLUTION
Fig. 3. Residuals extracted from least squares regression on Sciuroidea. The black bars are residuals for arboreal squirrels (n = 19), the hatched bars are
semiarboreal squirrels (n = 14), and the white bars are terrestrial squirrels (n = 18). Although the arboreal and terrestrial (P < 0.001) and arboreal and
semiarboreal (P = 0.032) intercepts are significantly different from each other, the semiarboreal and terrestrial intercepts are not (P > 0.05). OLS regression:
y = 0.1531x + 1.736, r2 = 0.241, P < 0.001.
Materials and Methods
size requirements (Table 1). Second, PIC (55, 56) were calculated and analyzed
on the entire dataset using the AOT function in Phylocom (57) to determine
the significance of habitat category on longevity and body mass after the
influence of phylogeny is removed (29).
Ordinary least squares (OLS) regression lines were fitted to the total
dataset and to the 10 relevant subgroups. ANCOVA tests were conducted on
the total dataset and on the subclades to determine whether intercepts for
habitat type are significantly different from each other using Bonferroni
posthoc tests. Because phylogenetic relationships can obscure the independence of data points (55, 56), the potential effects of phylogeny were
tested using the AOT function in Phylocom (57) to calculate and analyze PIC.
The AOT function is used to create PIC between continuous and categorical
traits. Because it is designed to work with a binary categorical variable, only
arboreal and terrestrial taxa are used in this portion of the analysis. Following Fisher and colleagues (29), we first calculated a set of PIC using only
the two continuous variables (body mass and longevity). Using these contrasts, we calculate the slope of the linear regression, m, with the intercept
forced through the origin. The equation for the regression line is then y =
mx. Next, a second set of PIC are calculated by contrasting body mass and
longevity against habitat type, creating body mass contrasts relative to
habitat (MR) and longevity contrasts relative to habitat (LR). The original
regression line obtained using only continuous variables (y = mx) then is
applied to the second set of contrasts to calculate residuals. This calculation
is accomplished by subtracting the longevity contrasts relative to habitat (LR)
from the product of the original slope (m) and the body mass contrasts
relative to habitat (MR). That is, residuals are calculated as mMR − LR. These
residuals then are subjected to a one-way t test to determine if they are
significantly different from zero. A significant result (P < 0.05) indicates that
habitat type has a significant effect on longevity relative to body mass.
Because two aspects of our phylogeny are controversial, namely Atlantogenata (58, 59) and Pegasoferae (60), we analyze independent contrasts
using modified phylogenies that do not recognize sister relationships
between Afrotheria and Xenarthra or Perrisodactyla and Ferae, in addition
to the main phylogeny presented in this analysis (Fig. 1 and Fig. S1).
Analyses were conducted on published data on 776 species, representing 24
orders from all major divisions of Mammalia (Fig. 1).The dataset for longevity was
compiled from published maximal lifespan records (48, 49). Both captive and
wild records are included; in fact, captive records are preferred, because maximum potential lifespan is of interest. Average adult body masses and habitat
categories (arboreal, semiarboreal, or terrestrial) were obtained from various
sources (48, 50–53). Although brain mass was once argued to be a better predictor of longevity than body mass in mammals (27), it has been demonstrated
that other body organ masses are equally or more highly correlated with longevity, suggesting that organ mass may be a better proxy for body size than
body mass (25, 28, 54). However, data for body mass are more widely available
than data for various organ masses; therefore, we use body mass as a covariate in
our study. Where quantitative data are available, the following criteria are used
to determine habitat type: 75–100% time spent in trees is considered arboreal,
25–75% time spent in trees is considered semiarboreal, and 0–25% time spent in
trees is considered terrestrial. However, for most species examined, this type of
information is not available (although many cases are obvious, such as many
“ungulates,” which are strictly terrestrial). For these species, categories are
determined based on qualitative descriptions. Those species described as
“arboreal/primarily arboreal” and “terrestrial/primarily terrestrial” are classified
arboreal and terrestrial, respectively; those described as “semiarboreal,” “semiterrestrial,” ”occasionally arboreal,” or ”arboreal and terrestrial” are classified
semiarboreal.
We constructed a mammalian supertree based on recently published
molecular phylogenies (Fig. 1 and Fig. S1). To control for the effects of shared
phylogenetic history, two methods were employed. First, several taxonomic
groups were analyzed independently using ANCOVA to determine whether
overall results were significantly influenced by one or a few subgroups.
Taxonomic groups were chosen so that they contained sufficient numbers of
arboreal and terrestrial species to conduct an ANCOVA. In some cases (e.g.,
Xenarthra), assumptions of ANCOVA are not met (slopes are not different
from zero), so there is no linear relationship between body mass and longevity,
presumably because of inadequate sample size for one or more habitat categories. Minimally, this analysis required at least three taxa in each category,
although in most cases the number was much higher (Table 1). Furthermore,
taxonomic groups were chosen to minimize redundancy. For example, the
group primates is not analyzed separately from Euarchonta because only
three nonprimate euarchontans are included in this dataset, and their inclusion (or exclusion) does not affect the results. Likewise, Carnivora and
Rodentia are not analyzed separately but rather are subsumed within the
larger clades Ferae (Carnivora + Pholidota) and Glires (Rodentia + Lagamorpha). In our dataset, 10 subclades are nonredundant and meet minimal sample
ACKNOWLEDGMENTS. We thank Steve Leigh, who encouraged, and whose
courses inspired, this project. We also thank Greg Blomquist, John Polk, and
Charles Roseman for valuable advice and discussions. Comments provided by
two anonymous reviewers greatly improved the manuscript. This work was
funded by a Cognitive Science/Artificial Intelligence Grant from the Beckman
Institute for Advanced Science and Technology, University of Illinois at
Urbana–Champaign.
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