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 survial 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 the...

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Published inEvolution Vol. 69; no. 12; pp. 3123 - 3140
Main Authors Tidière, Morgane, Gaillard, Jean-Michel, Müller, Dennis W. H., Lackey, Laurie Bingaman, Gimenez, Olivier, Clauss, Marcus, Lemaître, Jean-François
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.12.2015
Society for the Study of Evolution
Oxford University Press
Wiley
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Summary:In most mammals, both sexes display different survial 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.
Bibliography:ark:/67375/WNG-5VB9NNDG-F
Table S1. Longevity and actuarial senescence data in males (M) and females (F) of 60 ruminant species living in captivity. Table S2. Set of models fitted to explain variation in mean longevity and median longevity in ruminant males according to variation in diet, body mass (male BM), mating system (MS), and sexual size dimorphism (male BM + female BM). Table S3. Akaïke Information Criterion of model tested to describe sex-specific survival per age for each species of ruminant. Table S4. Metrics used to assess the onset of actuarial senescence. Table S5. Set of models fitted to explain variation in onsets of actuarial senescence of ruminant males, which were measured using 10 different metrics (seven original metrics + three synthetic metrics, cf. Table S4), according to variation in diet, body mass (male BM), mating system (MS), and sexual size dimorphism (male BM + female BM). Table S6. Set of models fitted to explain variation in onsets of actuarial senescence of ruminant females, which were measured using 10 different metrics (seven original metrics + three synthetics metrics, cf. Table S4), according to variation in diet, body mass (female BM), mating system (MS), and sexual size dimorphism (male BM + female BM). Table S7. Set of models fitted to explain variation in rates of senescence between six and 12 years of age and between six and nine years of age with or without including median longevity (MLm, male median longevity; MLf, female median longevity) as a covariate in analysis according to variation in diet, body mass (BMm, male body mass; BMf, female body mass), mating system (MS), and sexual size dimorphism (BMm + BMf). Table S8. Between-sex correlation of senescence and survival metrics. Table S9. Data on diet, mating system, mating tactic, body mass, and horn size (only for ruminant bovids) used in this study. Table S10. Models selected for each metric of survival and senescence of males depending on the SSD metric considered. Table S11. Set of models fitted to explain variation in survival and actuarial senescence metrics in males of ruminant cervid species in relation to variation in diet, body mass (male BM), sexual size dimorphism (male BM + female BM), and antler length (AL). Table S12. Set of models fitted to explain observed variation in longevity and metrics of actuarial senescence in ruminant males in relation to variation in diet, body mass (male BM), mating system (MS), and sexual size dimorphism (male BM + female BM). Table S13. Set of models fitted to test for a mating tactic effect on variation in longevity and actuarial senescence metrics in ruminant males (only polygynous and promiscuous species) in relation to variation in mating tactic (MT), body mass (male BM), and diet. Table S14. Parameter estimates from the models selected to assess the effects of mating tactic on longevity and senescence metrics in ruminant males (only polygynous and promiscuous species). Table S15. Set of models fitted to explain observed variation in longevity and metrics of actuarial senescence in males of ruminant bovid species in relation to variation in diet, body mass (male BM), horn size (male HS), sexual size dimorphism (male BM + female BM), and horn size dimorphism (male HS + female HS). Table S16. Set of models fitted to explain observed variation in longevity and metrics of actuarial senescence in ruminant females in relation to variation in diet, body mass (female BM), mating system (MS), and sexual size dimorphism (male BM + female BM) in ruminants. Table S17. Set of models fitted to test for a mating tactic effect on variation in longevity and actuarial senescence metrics in ruminant females (only polygynous and promiscuous species) in relation to variation in mating tactic (MT), body mass (female BM), and diet. Table S18. Set of models fitted to explain observed variation in longevity and metrics of actuarial senescence in females of ruminant bovid species in relation to variation in diet, body mass (female BM), horn size (female HS), sexual size dimorphism (male BM + female BM), and horn size dimorphism (male HS + female HS). Table S19. Set of models fitted to explain observed sex differences variation in longevity and metrics of actuarial senescence in relation to variation in body mass (BM), mating system (MS), and interaction between body mass and mating system (BM:MS) in ruminants. Table S20. Set of models fitted to explain observed sex-differences variation in longevity and metrics of actuarial senescence (only polygynous and promiscuous species) in relation to variation in mating tactic (MT), body mass (BM), and interaction between body mass and mating tactic (BM:MT) in ruminants. Table S21. Parameter estimates from the models selected to account for the effects of mating tactics on between-sex differences in four senescence and survival metrics of ruminants (only polygynous and promiscuous species). Table S22. Set of models fitted to explain observed sex-differences variation in longevity and metrics of actuarial senescence in ruminant bovid species in relation to variation in body mass dimorphism (male BM + female BM), horn size dimorphism (male HS + female HS), and interaction between body mass and horn size (male BM:male HS). Table S23. Models selected for each metric of survival and senescence of males depending on the SSD metric considered and in relation with or without correction for body mass and/or diet. Appendix S1. Method used to obtain the synthetic metric "median onset."Figure S1. Phylogenetic trees built on the 60 species of ruminants analyzed (based on Bininda-Emonds et al. 's [2007, 2008] phylogenetic tree) according to the percentage of grasses (A), mating system (B), and sexual size dimorphism (C). Figure S2. Log of age-specific mortality rate for males (in red) and females (in gray) of each ruminant species. Figure S3. Relationship among longevity DA0, Gompertz rate DB0, age at the onset of senescence DC0 or rate of senescence between six and 12 years of age DD0, and body mass in males of 60 ruminant species. Figure S4. Relationship among longevity DA', Gompertz rate DB', age at the onset of senescence DC' or rate of senescence between six and 12 years of age DD', and percentage of grass in species' natural diet in males of 60 ruminant species.
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ArticleID:EVO12801
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content type line 23
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ISSN:0014-3820
1558-5646
DOI:10.1111/evo.12801