Arboreality has allowed for the evolution of increased longevity in mammals

Abstract

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.

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, r ² = 0.499, P < 0.001. OLS regression for terrestrial mammals: y = 0.222x + 1.39, r ² = 0.756, P < 0.001.

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, r ² = 0.241, P < 0.001.

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, r ² = 0.594, P < 0.001.