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) The evolutionary theory of aging predicts that species will experi- other factors such as hibernation and reproductive rate have been ence delayed senescence and increased longevity when rates of shown to play a role in bat longevity (22), these factors are accordant extrinsic mortality are reduced. It has long been recognized that birds with evolutionary theory of aging, and it is clear that the exceptional and bats are characterized by lower rates of extrinsic mortality and longevity of Chiroptera as a whole is the result of flight. In addition to greater longevities than nonvolant endotherms, presumably be- flying birds and mammals, gliding mammals are longer-lived than cause flight reduces exposure to terrestrial predators, disease, and nonvolant, nongliding mammals (21, 23). As with flight and gliding environmental hazards. Like flight, arboreality may act to reduce behavior, arboreality may act to lower extrinsic mortality rates and extrinsic mortality, delay senescence, and increase longevity and has increase longevity by providing a relatively protected environment been suggested as an explanation for the long lifespans of primates. with reduced exposure to predation, disease, and environmental However, this hypothesis has yet to be tested in mammals in general. hazards. Indeed, Darwin himself (ref. 24, p. 169) identified an We analyze a large dataset of mammalian longevity records to test association between arboreality and extrinsic mortality, recognizing whether arboreal mammals are characterized by greater longevities the “power of quickly climbing trees, so as to escape from enemies.” than terrestrial mammals. Here, we show that arboreal mammals are Furthermore, several researchers have suggested that primates are longer lived than terrestrial mammals at common body sizes, inde- long-lived among mammals at least in part because they are largely pendent of phylogeny. Subclade analyses demonstrate that this arboreal (25, 26). If so, then we might expect arboreal mammals in trend holds true in nearly every mammalian subgroup, with two general to possess greater longevities than their terrestrial coun- — notable exceptions metatherians (marsupials) and euarchontans terparts. Using analysis of covariance (ANCOVA) and an analysis of EVOLUTION (primates and their close relatives). These subgroups are unique in phylogenetically independent contrasts (PIC), we test this hypoth- that each has experienced a long and persistent arboreal evolution- esis by comparing longevity records for arboreal and terrestrial ary history, with subsequent transitions to terrestriality occurring mammals in a molecular phylogenetic context (Fig. 1 and Fig. S1). multiple times within each group. In all other clades examined, ter- restriality appears to be the primitive condition, and species that Results and Discussion become arboreal tend to experience increased longevity, often inde- Overall, in agreement with previous studies (27, 28), body mass pendently in multiple lineages within each clade. Adoption of an accounts for 60% of the variance in maximal lifespan in nonvolant, arboreal lifestyle may have allowed for increased longevity in these nonaquatic mammals. Longevity, like many life-history traits, is fi lineages and in primates in general. Overall, these results con rm the negatively allometric, so that lifespan increases at between one- fundamental predictions of the evolutionary theory of aging. fourth and one-third the rate of body mass (Fig. 2). An initial analysis on the entire dataset indicates that the slope for semi- senescence | extrinsic mortality | terrestriality | marsupials | primates arboreal species is significantly different from the arboreal and terrestrial slopes. A separate analysis of Eutheria alone results in enescence, or aging, is an intrinsic biological phenomenon that common slopes for all three groups (see below; Table 1), suggesting Slimits an organism’s maximum potential lifespan, even in the that the departure of the semiarboreal slope results from the absence of extrinsic sources of mortality such as predation, disease, influence of marsupials. Because of this result, semiarboreal species and environmental hazards. Its evolution is of particular interest in were removed for analysis on the overall dataset, and an ANCOVA life-history studies (1, 2), in part because it is not immediately clear was conducted on the remaining habitat groups (arboreal and ter- why senescence persists in the presence of natural selection, which restrial). This analysis demonstrates that, at common body sizes, might be expected to eliminate it. The evolutionary theory of aging, arboreal mammals are characterized by greater longevities than in its several, nonmutually exclusive forms (3–8), proposes that terrestrial mammals (P < 0.001) (Table 1 and Fig. 2). Results of the senescence is the result of late-acting, deleterious mutations that PIC analysis on the mammalian dataset also are significant (P < accumulate because of the diminishing effectiveness of selection 0.001), indicating the effect of habitat type on longevity remains with increasing age. Extrinsic mortality is one major factor that even when the effects of phylogeny are removed. contributes to the accumulation of deleterious mutations by limiting Results of subsequent ANCOVA are listed in Table 1. In 8 of the exposure of these late-acting mutations to selection; thus, the evo- 10 subclades included in the analysis, arboreal mammals are char- lutionary theory of aging predicts that extrinsic mortality will be a acterized by greater longevities than terrestrial mammals (Table 1). principal determinate of the rate of senescence in age-structured Semiarboreal eutherian mammals are either intermediately long- populations (9). This theory predicts that populations experiencing lived or are not significantly different from one or the other habitat high extrinsic mortality rates will accumulate more deleterious type (Table 1 and Fig. 3). Results for two subclades, Metatheria mutations, evolve earlier senescence and reproduction, low somatic (marsupials) and Euarchonta (primates and their close relatives), maintenance, and shorter maximal lifespans. Conversely, pop- ulations subject to low extrinsic mortality rates will eliminate late- acting deleterious mutations more effectively and evolve delayed Author contributions: M.R.S. and S.A.W. designed research, performed research, analyzed senescence, late fecundity, durable somas, and greater longevities. data, and wrote the paper. These relationships have been demonstrated in laboratory (10–12), The authors declare no conflict of interest. wild (13–15), and simulation (16) studies. This article is a PNAS Direct Submission. In the wild, flying birds and bats experience lower rates of extrinsic 1To whom correspondence should be addressed. E-mail: [email protected]. – mortality(17)andgreaterlongevity(1823) than their nonvolant This article contains supporting information online at www.pnas.org/cgi/content/full/ relatives, presumably because of decreased predation. Although 0911439107/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.0911439107 PNAS Early Edition | 1of5 Downloaded by guest on September 24, 2021 Prototheria Mammalia Metatheria Atlantogenata Afrotheria Theria Xenarthra Eutheria Euarchonta Euarchontoglires Glires Eulipotyphla Boreoeutheria Cetartiodactyla Laurasiatheria Chiroptera Ferae Pegasoferae Perissodactyla Fig. 1. Molecular phylogeny of Mammalia. Prototheria: monotremes. Meta- theria: marsupials. Afrotheria: aardvark, tenrecs, elephant shrews, hyraxes, manatees, dugongs, elephants. Xenarthra: sloths, anteaters, armadillos. Euarchonta: tree shrews, colugos, primates. Glires: rodents, rabbits. Eulipoty- phla: moles, hedgehogs, shrews. Cetartiodactyla: bovids, cervids, suiforms, camelids, hippopotamids, cetaceans. Chiroptera: bats. Ferae: Pholidota (manids) Fig. 2. Maximal lifespan plotted against body mass for 776 mammals in log and Carnivora (canids, ursids, musteloids, pinnipeds, felids, viverrids, herpestids, space. The solid line is the least squares regression for terrestrial mammals; hyaenids). Perissodactyla: horses, tapirs, rhinos. the dashed line is the least squares regression for arboreal mammals. The slopes for these regression lines are common, and the intercepts are sig- nificantly different (P < 0.001). OLS regression for arboreal mammals: y = differfromthe overall results. Within Metatheria, although arboreal 0.245x + 1.64, r2 = 0.499, P < 0.001. OLS regression for terrestrial mammals: 2 < and terrestrial marsupials are not significantly different from each y = 0.222x + 1.39, r = 0.756, P 0.001. other, both are significantly longer-lived than semiarboreal taxa (Table 1). Our results therefore confirm a previous finding that primates, initially evolved in an ancestral euarchontan (30–35). arboreality is not associated with increased longevity in marsupials Marsupials also probably are primitively arboreal (34, 36–38), (29). In Euarchonta, our analyses did not reveal significant differ- ences between any of the habitat types (Table 1). However, taken with subsequent and repeated events of terrestriality (38). In together, the overall results demonstrate that there is a general, contrast,