Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants

In most mammals, both sexes display different survival patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age‐specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

[1]  Lena Osterhagen Adaptation And Natural Selection A Critique Of Some Current Evolutionary Thought , 2016 .

[2]  J. Gaillard,et al.  Early-late life trade-offs and the evolution of ageing in the wild , 2015, Proceedings of the Royal Society B: Biological Sciences.

[3]  J. Gaillard,et al.  Males do not senesce faster in large herbivores with highly seasonal rut , 2014, Experimental Gerontology.

[4]  J. Gaillard,et al.  Do age‐specific survival patterns of wild boar fit current evolutionary theories of senescence? , 2014, Evolution; international journal of organic evolution.

[5]  J. Gaillard,et al.  Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer , 2014, Proceedings of the Royal Society B: Biological Sciences.

[6]  M. Clauss,et al.  A test of the metabolic theory of ecology with two longevity data sets reveals no common cause of scaling in biological times , 2014 .

[7]  R. Bonduriansky,et al.  Sexual conflict, life span, and aging. , 2014, Cold Spring Harbor perspectives in biology.

[8]  J. Dutheil,et al.  Mitochondrial DNA as a tool for reconstructing past life‐history traits in mammals , 2014, Journal of evolutionary biology.

[9]  The allometry between secondary sexual traits and body size is nonlinear among cervids , 2014, Biology Letters.

[10]  J. Vaupel,et al.  Diversity of ageing across the tree of life , 2013, Nature.

[11]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[12]  T. Burke,et al.  The impact of reproductive investment and early‐life environmental conditions on senescence: support for the disposable soma hypothesis , 2013, Journal of evolutionary biology.

[13]  V. Lummaa,et al.  Evolution of sex differences in lifespan and aging: Causes and constraints , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[14]  L. Partridge,et al.  Gender and longevity: why do men die earlier than women? Comparative and experimental evidence. , 2013, Best practice & research. Clinical endocrinology & metabolism.

[15]  J. Gaillard,et al.  Polyandry Has No Detectable Mortality Cost in Female Mammals , 2013, PloS one.

[16]  J. Gaillard,et al.  Male survival patterns do not depend on male allocation to sexual competition in large herbivores , 2013 .

[17]  J. Gaillard,et al.  Comparing free-ranging and captive populations reveals intra-specific variation in aging rates in large herbivores , 2013, Experimental Gerontology.

[18]  Jean-Michel Gaillard,et al.  Senescence in natural populations of animals: Widespread evidence and its implications for bio-gerontology , 2013, Ageing Research Reviews.

[19]  D. Promislow,et al.  A comparative assessment of univariate longevity measures using zoological animal records , 2012, Aging cell.

[20]  M. Clauss,et al.  Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history , 2012, Biological reviews of the Cambridge Philosophical Society.

[21]  Longevity in Bovids Is Promoted by Sociality, But Reduced by Sexual Selection , 2012, PloS one.

[22]  O. Jones,et al.  BaSTA: an R package for Bayesian estimation of age‐specific survival from incomplete mark–recapture/recovery data with covariates , 2012 .

[23]  J. Fritz,et al.  Dichotomy of eutherian reproduction and metabolism , 2012 .

[24]  J. Gaillard,et al.  Revisiting the allometry of antlers among deer species: male-male sexual competition as a driver , 2011 .

[25]  G. Wagner,et al.  Measurement and Meaning in Biology , 2011, The Quarterly Review of Biology.

[26]  M. Clauss,et al.  Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants , 2011, Proceedings of the Royal Society B: Biological Sciences.

[27]  J. Bro-Jørgensen Intra- and Intersexual Conflicts and Cooperation in the Evolution of Mating Strategies: Lessons Learnt From Ungulates , 2011, Evolutionary Biology.

[28]  Liam J. Revell,et al.  Phylogenetic signal and linear regression on species data , 2010 .

[29]  J. Gaillard,et al.  Age at the onset of senescence in birds and mammals is predicted by early-life performance , 2010, Proceedings of the Royal Society B: Biological Sciences.

[30]  R. Ricklefs,et al.  Life-history connections to rates of aging in terrestrial vertebrates , 2010, Proceedings of the National Academy of Sciences.

[31]  M. Murray The Rut of Impala: Aspects of Seasonal Mating under Tropical Conditions , 2010 .

[32]  M. Bérubé,et al.  Sex-specific survival in the humpback whale Megaptera novaeangliae in the Gulf of St. Lawrence, Canada , 2010 .

[33]  R. Freckleton The seven deadly sins of comparative analysis , 2009, Journal of evolutionary biology.

[34]  Roger Pradel,et al.  Program E-Surge: A Software Application for Fitting Multievent Models , 2009 .

[35]  Kate E. Jones,et al.  Erratum: The delayed rise of present-day mammals , 2008 .

[36]  I. Agnarsson,et al.  The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. , 2008, Molecular phylogenetics and evolution.

[37]  J. Gaillard,et al.  Senescence rates are determined by ranking on the fast-slow life-history continuum. , 2008, Ecology letters.

[38]  R. Ricklefs,et al.  The evolutionary ecology of senescence , 2008 .

[39]  R. Bonduriansky,et al.  Sexual selection, sexual conflict and the evolution of ageing and life span , 2008 .

[40]  J. Gaillard,et al.  Measuring senescence in wild animal populations: towards a longitudinal approach , 2008 .

[41]  G. Sacher,et al.  Relation of Lifespan to Brain Weight and Body Weight in Mammals , 2008 .

[42]  J. Gaillard,et al.  Vertebrate Ageing: An Evolutionary Process with a Genetic Basis? , 2008, Current Biology.

[43]  T. Clutton‐Brock,et al.  Sex differences in ageing in natural populations of vertebrates , 2007, Proceedings of the Royal Society B: Biological Sciences.

[44]  D. Irschick,et al.  The Evolution of Performance‐Based Male Fighting Ability in Caribbean Anolis Lizards , 2007, The American Naturalist.

[45]  J. Gaillard,et al.  Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic. , 2007, The Journal of animal ecology.

[46]  J. Bro-Jørgensen THE INTENSITY OF SEXUAL SELECTION PREDICTS WEAPON SIZE IN MALE BOVIDS , 2007, Evolution; international journal of organic evolution.

[47]  Joseph B. Williams,et al.  Tropical birds have a slow pace of life , 2007, Proceedings of the National Academy of Sciences.

[48]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[49]  Jean-Michel Gaillard,et al.  Generation Time: A Reliable Metric to Measure Life‐History Variation among Mammalian Populations , 2005, The American Naturalist.

[50]  T. Székely,et al.  MORTALITY COSTS OF SEXUAL SELECTION AND PARENTAL CARE IN NATURAL POPULATIONS OF BIRDS , 2005, Evolution; international journal of organic evolution.

[51]  A. Herrel,et al.  Does dewlap size predict male bite performance in Jamaican Anolis lizards , 2005 .

[52]  T. Clutton‐Brock,et al.  Does environmental stochasticity matter? Analysis of red deer life-histories on Rum , 1995, Evolutionary Ecology.

[53]  S. Austad,et al.  Senescence in Wild Populations of Mammals and Birds , 2005 .

[54]  J. Gaillard,et al.  Assessing senescence patterns in populations of large mammals , 2004, Animal Biodiversity and Conservation.

[55]  T. Caro,et al.  Correlates of horn and antler shape in bovids and cervids , 2003, Behavioral Ecology and Sociobiology.

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

[57]  J. Gaillard,et al.  Variable age structure and apparent density dependence in survival of adult ungulates. , 2003, The Journal of animal ecology.

[58]  J. Gaillard,et al.  Causes of sex‐biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? , 2003 .

[59]  D. Coltman,et al.  Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  J. Gaillard,et al.  Ecological Correlates of Life Span in Populations of Large Herbivorous Mammals , 2003 .

[61]  M. Pagel,et al.  Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence , 2002, The American Naturalist.

[62]  Robert P. Freckleton,et al.  On the misuse of residuals in ecology: regression of residuals vs. multiple regression , 2002 .

[63]  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.

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

[65]  J. Gaillard,et al.  Temporal Variation in Fitness Components and Population Dynamics of Large Herbivores , 2000 .

[66]  Marco Festa-Bianchet,et al.  AGE‐SPECIFIC SURVIVAL IN FIVE POPULATIONS OF UNGULATES: EVIDENCE OF SENESCENCE , 1999 .

[67]  J. Gaillard,et al.  What factors shape sexual size dimorphism in ungulates , 1999 .

[68]  F. Weckerly Sexual-Size Dimorphism: Influence of Mass and Mating Systems in the Most Dimorphic Mammals , 1998 .

[69]  I. Owens,et al.  Mortality costs of parental care and sexual dimorphism in birds , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  J. Gaillard,et al.  SENESCENCE IN NATURAL POPULATIONS OF MAMMALS: A REANALYSIS , 1994, Evolution; international journal of organic evolution.

[71]  Roger Pradel,et al.  Roe deer survival patterns: a comparative analysis of contrasting populations , 1993 .

[72]  R. Montgomerie,et al.  Mortality costs of sexual dimorphism in birds , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[73]  D. Promislow Costs of sexual selection in natural populations of mammals , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  David R. Anderson,et al.  Modeling Survival and Testing Biological Hypotheses Using Marked Animals: A Unified Approach with Case Studies , 1992 .

[75]  J. Lovich,et al.  A review of techniques for quantifying sexual size dimorphism. , 1992, Growth, development, and aging : GDA.

[76]  J. Nichols,et al.  Model-based estimates of annual survival rate are preferable to observed maximum lifespan statistics for use in comparative life-history studies , 1989 .

[77]  J. Gaillard,et al.  An analysis of demographic tactics in birds and mammals , 1989 .

[78]  T. Clutton‐Brock Review Lecture: Mammalian mating systems , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

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

[80]  P. Jarman MATING SYSTEM AND SEXCUL DIMORPHISM IN LARGE TERRESTRIAL, MAMMALIAN HERBIVORES , 1983 .

[81]  N. Owen‐Smith On Territoriality in Ungulates and an Evolutionary Model , 1977, The Quarterly Review of Biology.

[82]  V. Geist THE EVOLUTIONARY SIGNIFICANCE OF MOUNTAIN SHEEP HORNS , 1966, Evolution; international journal of organic evolution.

[83]  Bateman Aj Intra-sexual selection in Drosophila. , 1948 .

[84]  A. Bateman,et al.  Intra-sexual selection in Drosophila , 1948, Heredity.

[85]  N. Pierce Origin of Species , 1914, Nature.

[86]  R. Meldola Sexual Selection , 1871, Nature.