Life-history connections to rates of aging in terrestrial vertebrates

The actuarial senescence (i.e., the rate of increase in adult mortality with age) was related to body mass, development period, and age at sexual maturity across 124 taxonomic families of terrestrial vertebrates. Model selection based on Akaike's information criterion values adjusted for small size showed that the rate of aging decreases with increasing body mass, gestation period, age at maturity, and possession of flight. Among families of mammals, actuarial senescence was related to extrinsic mortality rate (standardized regression coefficient = 0.215), gestation period (−0.217), and age at maturity (−0.553). Although rate of aging in birds also was related to the embryo development period, birds grow several times more rapidly than mammals, and therefore, the connection between rate of early development and rate of aging is unclear. The strong vertebrate-wide relationship between rate of aging, or life span, and age at maturity can be explained by density-dependent feedback of adult survival rate on the recruitment of young individuals into the breeding population. Thus, age at maturity seems to reflect extrinsic mortality, which, in turn, influences selection on mechanisms that postpone physiological and actuarial senescence. Because rate of embryo development influences rate of aging independently of the age at maturity, in a statistical sense, the evolutionary diversification of development and aging seem to be connected in both birds and mammals; however, the linking mechanisms are not known.

[1]  R. Ricklefs Embryo growth rates in birds and mammals , 2010 .

[2]  R. Ricklefs,et al.  Biological implications of the Weibull and Gompertz models of aging. , 2002, The journals of gerontology. Series A, Biological sciences and medical sciences.

[3]  J. Prothero Adult life span as a function of age at maturity , 1993, Experimental Gerontology.

[4]  L. Partridge,et al.  Insulin/IGF-like signalling, the central nervous system and aging. , 2009, The Biochemical journal.

[5]  Hans-Georg Müller,et al.  Age of ovary determines remaining life expectancy in old ovariectomized mice , 2003, Aging cell.

[6]  D. J. Waters,et al.  Exploring mechanisms of sex differences in longevity: lifetime ovary exposure and exceptional longevity in dogs , 2009, Aging cell.

[7]  R. Ricklefs,et al.  Lifespan is unrelated to investment in reproduction in populations of mammals and birds in captivity. , 2007, Ecology letters.

[8]  L. Partridge,et al.  Evolution of aging: Testing the theory usingDrosophila , 1993, Genetica.

[9]  T. Kirkwood,et al.  The evolution of ageing and longevity , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[10]  Eric L. Charnov,et al.  Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology , 1993 .

[11]  J. Mcglade,et al.  Advanced ecological theory : principles and applications , 1999 .

[12]  Thomas E. Johnson,et al.  Evolutionary biology of aging , 1990 .

[13]  J. de Magalhães,et al.  A database of vertebrate longevity records and their relation to other life‐history traits , 2009, Journal of evolutionary biology.

[14]  João Pedro de Magalhães,et al.  An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. , 2007, The journals of gerontology. Series A, Biological sciences and medical sciences.

[15]  R. Ricklefs Intrinsic aging-related mortality in birds , 2000 .

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

[17]  Evolutionarily stable age at first reproduction in a density-dependent model. , 1992, Journal of theoretical biology.

[18]  Peter Calow,et al.  Physiological Ecology: An Evolutionary Approach to Resource Use , 1983 .

[19]  L. Partridge,et al.  Endocrine regulation of aging and reproduction in Drosophila , 2009, Molecular and Cellular Endocrinology.

[20]  E. Martins The Comparative Method in Evolutionary Biology, Paul H. Harvey, Mark D. Pagel. Oxford University Press, Oxford (1991), vii, + 239 Price $24.95 paperback , 1992 .

[21]  C. Carter,et al.  A critical analysis of the role of growth hormone and IGF-1 in aging and lifespan. , 2002, Trends in genetics : TIG.

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

[23]  Scott A. Williams,et al.  Arboreality has allowed for the evolution of increased longevity in mammals , 2010, Proceedings of the National Academy of Sciences.

[24]  Robert S. Balaban,et al.  Mitochondria, Oxidants, and Aging , 2005, Cell.

[25]  Eileen M. Crimmins,et al.  Inflammatory Exposure and Historical Changes in Human Life-Spans , 2004, Science.

[26]  B. Charlesworth Evolutionary mechanisms of senescence , 2005, Genetica.

[27]  J. Millar,et al.  Life Histories of Mammals: An Analysis of Life Tables , 1983 .

[28]  N. Stenseth,et al.  Mechanisms for delayed density-dependent reproductive traits in field voles, Microtus agrestis: the importance of inherited environmental effects , 2001 .

[29]  B. Sæther,et al.  AVIAN LIFE HISTORY VARIATION AND CONTRIBUTION OF DEMOGRAPHIC TRAITS TO THE POPULATION GROWTH RATE , 2000 .

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

[31]  L. Gavrilov,et al.  The biology of life span: A quantitative approach: Revised and updated English edition. Originally published in Russian by Nauka, Moscow, 1986. Translated into English by John and Liliya Payne. 385 pp., 1991. Price: $40.00 US , 1992 .

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

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

[34]  R. Ricklefs,et al.  Comparison of aging-related mortality among birds and mammals , 2001, Experimental Gerontology.

[35]  P. Monaghan,et al.  Do telomere dynamics link lifestyle and lifespan? , 2006, Trends in ecology & evolution.

[36]  E. Charnov On evolution of age of maturity and the adult lifespan , 1990 .

[37]  D. Winkler,et al.  Telomerase activity is maintained throughout the lifespan of long-lived birds , 2007, Experimental Gerontology.

[38]  S. Wright,et al.  The Rate Of Living , 2011 .

[39]  Martin Wikelski,et al.  The physiology/life-history nexus , 2002 .

[40]  C. Kahn,et al.  Endocrine regulation of ageing , 2007, Nature Reviews Molecular Cell Biology.

[41]  S. J. Olshansky,et al.  The Biology of Life Span: A Quantitative Approach. , 1992 .

[42]  G. Martin,et al.  The genetics of aging. , 2003, Annual review of genomics and human genetics.

[43]  S. Austad Diverse aging rates in metazoans: targets for functional genomics , 2005, Mechanisms of Ageing and Development.

[44]  F. T. Jung The Fire of Life , 1962 .

[45]  S. Stearns,et al.  The Evolution of Life Histories , 1992 .

[46]  G. Barja Aging in vertebrates, and the effect of caloric restriction: a mitochondrial free radical production–DNA damage mechanism? , 2004, Biological reviews of the Cambridge Philosophical Society.

[47]  R. Ricklefs On the Evolution of Reproductive Strategies in Birds: Reproductive Effort , 1977, The American Naturalist.

[48]  T. Prolla,et al.  The Role of Mitochondrial DNA Mutations in Mammalian Aging , 2007, PLoS genetics.

[49]  David L. Wilson,et al.  The analysis of survival (mortality) data: Fitting Gompertz, Weibull, and logistic functions , 1994, Mechanisms of Ageing and Development.

[50]  R. Ricklefs DENSITY DEPENDENCE, EVOLUTIONARY OPTIMIZATION, AND THE DIVERSIFICATION OF AVIAN LIFE HISTORIES , 2000 .

[51]  D. Promislow SENESCENCE IN NATURAL POPULATIONS OF MAMMALS: A COMPARATIVE STUDY , 1991, Evolution; international journal of organic evolution.

[52]  E. Charnov A note on dimensionless life histories for birds versus mammals , 1995, Evolutionary Ecology.

[53]  P. Sherman,et al.  Avian longevities and their interpretation under evolutionary theories of senescence , 2010 .

[54]  W. Calder The comparative biology of longevity and lifetime energetics , 1985, Experimental Gerontology.

[55]  R. Ricklefs Insights from comparative analyses of aging in birds and mammals , 2010, Aging cell.

[56]  D. Promislow,et al.  On size and survival: progress and pitfalls in the allometry of life span. , 1993, Journal of gerontology.

[57]  W. Calder Size, Function, and Life History , 1988 .

[58]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[59]  Manuel Serrano,et al.  The common biology of cancer and ageing , 2007, Nature.

[60]  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.