Abstract
Extra-pair paternity (EPP) is often linked to male age in socially monogamous vertebrates; that is, older males are more likely to gain EPP and less likely to be cuckolded. However, whether this occurs because males improve at gaining paternity as they grow older, or because "higher quality" males that live longer are preferred by females, has rarely been tested, despite being central to our understanding of the evolutionary drivers of female infidelity. Moreover, how extra-pair reproduction changes with age within females has received even less attention. Using 18years of longitudinal data from an individually marked population of Seychelles warblers (Acrocephalus sechellensis), we found considerable within-individual changes in extra-pair reproduction in both sexes: an early-life increase and a late-life decline. Furthermore, males were cuckolded less as they aged. Our results indicate that in this species age-related patterns of extra-pair reproduction are determined by within-individual changes with age, rather than differences among individuals in longevity. These results challenge the hypothesis-based on longevity reflecting intrinsic quality-that the association between male age and EPP is due to females seeking high-quality paternal genes for offspring. Importantly, EPP accounted for up to half of male reproductive success, emphasizing the male fitness benefits of this reproductive strategy. Finally, the occurrence of post-peak declines in extra-pair reproduction provides explicit evidence of senescence in infidelity in both males and females.
Highlights
Across socially monogamous species, levels of extra-pair paternity (EPP) show that infidelity occurs frequently, yet the evolution of this behaviour remains enigmatic (Griffith, Owens, & Thuman, 2002; Taylor, Price, & Wedell, 2014; Westneat& Stewart, 2003)
We found no evidence of a trade-off between extra-group paternity (EGP) and within-group paternity (WGP): WGP and its interaction with male age were not related to EGP success, and EGP and its interaction with male age did not predict WGP success (Table 4)
In the Seychelles warbler, we found that male paternity gain varied with age within individuals, and that age-related changes were not explained by selective appearance or disappearance effects
Summary
Levels of extra-pair paternity (EPP) show that infidelity (i.e., extra-pair mating) occurs frequently, yet the evolution of this behaviour remains enigmatic Contrary to the good genes hypothesis, the competitive ability hypothesis predicts a within-male age effect and does not imply any indirect genetic benefits for females These two hypotheses are not mutually exclusive because both within- and between-individual differences in EPP in relation to age may occur at the same time. In a good genes scenario, the oldest males are the most attractive because they are of highest intrinsic quality (as evidenced by highest longevity) and are preferred by females; if senescence causes lower fertilization ability (e.g., because of lower sperm competitiveness; Dean et al, 2010), very old males may gain less extra-pair (and total) paternity than younger (less attractive) males In this case, annual EPP success would be impacted by both a between-individual age effect, represented by a positive association between annual EPP and longevity (because males that live longer are preferred by females),. By undertaking the analyses outlined above, we provide evidence to distinguish between different hypotheses as to why females engage in extra-pair mating and improve our understanding of the factors driving the evolution of infidelity
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