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.senescence | extrinsic mortality | terrestriality | marsupials | primates S 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...

Ecology and mode-of-life explain lifespan variation in birds and mammals

“…The relationship between arboreality and extended lifespan in mammals has been shown previously [17], but to the best of our knowledge this is the first comparative analysis of lifespan in fossorial versus non-fossorial species. Our results may, therefore, offer a partial explanation for the exceptional longevity of naked mole rats (Heterocephalus glaber) which are completely fossorial and live 10 times longer than expected, given their body size [21].…”

“…Previous studies have investigated the relationship between lifespan and various ecological variables, but most only investigated select groups of species and few considered multiple traits simultaneously (e.g. [17]). …”

“…species which feed in trees, water or aerially) will live longer than terrestrial foragers, because they will be more capable of escaping from predators than species that feed on the ground [13,17,20]; and (iv) fossorial (i.e. species that live in permanent burrows) and semi-fossorial species will live longer than purely terrestrial species, because they possess means to escape predation and unfavourable conditions through refuge [21].…”

Explaining brain size variation: from social to cultural brain

“…(Note that the body-size effect mentioned above may be compounded by this life-history effect.) Because primates, including apes, have a long history of arboreality and were thus subject to lower predation rates than terrestrial mammals of similar body size [35,41], they could afford to evolve larger brains. Thus, the life-history filter produces grade shifts because environmental conditions that determine unavoidable mortality prevent potential improvements due to cognitive solutions from being expressed.…”

Diet mediates the relationship between longevity and reproduction in mammals

“…In some species, high levels of extrinsic mortality due to disease, predation, or abiotic pressures may result in low levels of selection for longevity-enhancing traits, which would not have a chance to be expressed in nature (Williams 1957;Williams et al 2006;Ricklefs 2010). This extrinsic mortality hypothesis has been used to explain the significantly higher lifespans of flying or arboreal animals, especially birds and bats, which may have lower mortality due to predation compared to similarly sized non-flying animals (Austad and Fischer 1991;Wilkinson and South 2002;Shattuck and Williams 2010;Wasser and Sherman 2010).…”