Arboreality has allowed for the evolution of increased longevity in mammals

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.

[1]  C. Darwin The Descent of Man and Selection in Relation to Sex: INDEX , 1871 .

[2]  P. Pye-Smith The Descent of Man, and Selection in Relation to Sex , 1871, Nature.

[3]  B. Bensley On the Question of an Arboreal Ancestry of the Marsupialia, and the Interrelationships of the Mammalian Subclasses , 1901, The American Naturalist.

[4]  G. E. Smith Arboreal Man , 1917, Nature.

[5]  George C. Williams,et al.  PLEIOTROPY, NATURAL SELECTION, AND THE EVOLUTION OF SENESCENCE , 1957, Science of Aging Knowledge Environment.

[6]  F. Bourliére The Comparative Biology of Aging , 1958 .

[7]  R. Haines Arboreal or Terrestrial Ancestry of Placental Mammals , 1958, The Quarterly Review of Biology.

[8]  J. E. Harker DIURNAL RHYTHMS IN THE ANIMAL KINGDOM , 1958 .

[9]  W. Hamilton The moulding of senescence by natural selection. , 1966, Journal of theoretical biology.

[10]  R. Nowak,et al.  Walker's mammals of the world , 1968 .

[11]  J. H. Kaufmann The Ecology and Evolution of Social Organization in the Kangaroo Family (Macropodidae) , 1974 .

[12]  T. Kirkwood Evolution of ageing , 1977, Nature.

[13]  A. C. Economos Brain-life span conjecture: a reevaluation of the evidence. , 1980, Gerontology.

[14]  J. E. Cronin,et al.  Comparative Biology and Evolutionary Relationships of Tree Shrews , 1981, Advances in Primatology.

[15]  B. Charlesworth,et al.  Genetics of life history in Drosophila melanogaster. II. Exploratory selection experiments. , 1981, Genetics.

[16]  B. Grzimek,et al.  Grzimek's Animal Life Encyclopedia , 1984 .

[17]  C. Pond,et al.  Walker's Mammals of the World, 4th Edition, Ronald M. Nowak, John L. Paradiso. The Johns Hopkins University Press, Baltimore, Maryland (1983), 1xi, +1-568 (Vol. I), xxv+569-1362 (Vol. II). Price $65.00 , 1984 .

[18]  L. Luckinbill,et al.  SELECTION FOR DELAYED SENESCENCE IN DROSOPHILA MELANOGASTER , 1984, Evolution; international journal of organic evolution.

[19]  Paul H. Harvey,et al.  Patterns of mortality and age at first reproduction in natural populations of mammals , 1985, Nature.

[20]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[21]  J. Prothero,et al.  Scaling of maximal lifespan in bats. , 1987, Comparative biochemistry and physiology. A, Comparative physiology.

[22]  K. H. Thompson,et al.  Evolution of Longevity in Animals , 1987, Springer US.

[23]  M. Dagosto Implications of postcranial evidence for the origin of euprimates , 1988 .

[24]  Paul H. Harvey,et al.  Living fast and dying young: A comparative analysis of life‐history variation among mammals , 1990 .

[25]  D. Pomeroy Why fly? The possible benefits for lower mortality , 1990 .

[26]  Robert W. Sussman,et al.  Primate origins and the evolution of angiosperms , 1991, American journal of primatology.

[27]  S. Austad,et al.  Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. , 1991, Journal of gerontology.

[28]  T. Garland,et al.  Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts , 1992 .

[29]  Steven N. Austad,et al.  Primate longevity: Its place in the mammalian scheme , 1992, American journal of primatology.

[30]  P. Jarman,et al.  Macropod Studies at Wallaby Creek. IX*. Exposure and Responses of Eastern Grey Kangaroos to Dingoes , 1993 .

[31]  S. Austad Retarded senescence in an insular population of Virginia opossums (Didelphis virginiana) , 1993 .

[32]  L. Partridge,et al.  Optimally, mutation and the evolution of ageing , 1993, Nature.

[33]  S. Austad,et al.  Fly Now, Die Later: Life-History Correlates of Gliding and Flying in Mammals , 1994 .

[34]  C. Janson,et al.  Predicting group size in primates: foraging costs and predation risks , 1995 .

[35]  B. Charlesworth,et al.  Evolution in Age-Structured Populations. , 1995 .

[36]  N. Rowe The Pictorial Guide to the Living Primates , 1996 .

[37]  R. J. Smith,et al.  Body mass in comparative primatology. , 1997, Journal of human evolution.

[38]  R. Ricklefs Evolutionary Theories of Aging: Confirmation of a Fundamental Prediction, with Implications for the Genetic Basis and Evolution of Life Span , 1998, The American Naturalist.

[39]  Steven N. Austad,et al.  Why do we age? , 2000, Nature.

[40]  M. Doebeli,et al.  Experimental evolution of aging, growth, and reproduction in fruitflies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Christopher N. Johnson,et al.  THE ECOLOGICAL BASIS OF LIFE HISTORY VARIATION IN MARSUPIALS , 2001 .

[42]  G. Wilkinson,et al.  Life history, ecology and longevity in bats , 2002, Aging cell.

[43]  Arthur J. Robson,et al.  The emergence of humans: The coevolution of intelligence and longevity with intergenerational transfers , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[44]  S. K. Morgan Ernest,et al.  LIFE HISTORY CHARACTERISTICS OF PLACENTAL NONVOLANT MAMMALS , 2003 .

[45]  Zhe‐Xi Luo,et al.  An Early Cretaceous Tribosphenic Mammal and Metatherian Evolution , 2003, Science.

[46]  J. L. Gittleman Carnivore body size: Ecological and taxonomic correlates , 1985, Oecologia.

[47]  L. Isbell Predation on primates: Ecological patterns and evolutionary consequences , 2005 .

[48]  Richard Weigl Longevity of mammals in captivity: From the Living Collections of the world. A list of mammalian longevity in captivity , 2005 .

[49]  M. Hasegawa,et al.  Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Marina Cords,et al.  Primates in Perspective , 2010, International Journal of Primatology.

[51]  M. Ravosa,et al.  PRIMATE ORIGINS: Adaptations and evolution , 2007 .

[52]  Webb Miller,et al.  Using genomic data to unravel the root of the placental mammal phylogeny. , 2007, Genome research.

[53]  Bruno Nyffeler,et al.  Early History of Mammals Is Elucidated with the ENCODE Multiple Species Sequencing Data , 2007, PLoS genetics.

[54]  P. Cahan,et al.  A High-Resolution Map of Segmental DNA Copy Number Variation in the Mouse Genome , 2006, PLoS genetics.

[55]  D. Boyer,et al.  Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms. , 2008, Journal of human evolution.

[56]  V. Weisbecker,et al.  PARALLEL EVOLUTION OF HAND ANATOMY IN KANGAROOS AND VOMBATIFORM MARSUPIALS: FUNCTIONAL AND EVOLUTIONARY IMPLICATIONS , 2008 .

[57]  N. Wolf Comparative biology of aging , 2009 .

[58]  T. Clutton‐Brock,et al.  Primate ecology and social organization , 2009 .