The contribution of extra‐pair paternity to the variation in lifetime and age‐specific male reproductive success in a socially monogamous species

Abstract

In socially monogamous species, extra-pair paternity (EPP) is predicted to increase variance in male reproductive success (RS) beyond that resulting from genetic monogamy, thus, increasing the "opportunity for selection" (maximum strength of selection that can act on traits). This prediction is challenging to investigate in wild populations because lifetime reproduction data are often incomplete. Moreover, age-specific variances in reproduction have been rarely quantified. We analyzed 21 years of near-complete social and genetic reproduction data from an insular population of Seychelles warblers (Acrocephalus sechellensis). We quantified EPP's contribution to lifetime and age-specific opportunities for selection in males. We compared the variance in male genetic RS vs social ("apparent") RS (RS ap ) to assess if EPP increased the opportunity for selection over that resulting from genetic monogamy. Despite not causinga statistically significant excess (19%) of the former over the latter, EPP contributed substantially (27%) to the variance in lifetime RS, similarly to within-pair paternity (WPP, 39%) and to the positive WPP-EPP covariance (34%). Partitioning the opportunity for selection into age-specific (co)variance components, showed that EPP also provided a substantial contribution at most ages, varying with age. Therefore, despite possibly not playing the main role in shaping sexual selection in Seychelles warblers, EPP provided a substantial contribution to the lifetime and age-specific opportunity for selection, which can influence evolutionary processes in age-structured populations.

Divorce is linked with extra‐pair paternity in a monogamous passerine

“…Previous studies into the link between divorce and extra‐pair behaviour are few and often conflicting (Ramsay et al 2000), but a recent meta‐analysis across species suggested that the rate of divorce is significantly linked with male, but not female, promiscuity (Chen et al 2023). The male perspective on divorce and extra‐pair paternity was beyond the scope of this study (Lebigre et al 2013, Girndt et al 2018, Raj Pant et al 2022).…”

“…More often, extra‐pair males, those from outside an established pair bond, only have the potential to provide indirect benefits to females. That is, extra‐pair males sire offspring without investing in costly parental care (Arnqvist and Kirkpatrick 2005, Lebigre et al 2013, Raj Pant et al 2022, Table 1). The good‐genes hypothesis predicts that extra‐pair males should therefore signal a better (Hamilton and Zuk 1982, Birkhead 1995, Kirkpatrick and Barton 1997), or more compatible (Blomqvist et al 2002, Griffith and Immler 2009, Ihle et al 2015), genetic proposition than the social partner.…”

The costs of extra-pair mating

“…Loss of paternity is a direct cost of EPP, as it reduce the number of offspring produced [5]. Although studies have investigated the fitness benefits of obtaining EPP [44], fewer have investigated the reduced fitness due to loss of paternity (i.e. the reduced lifetime reproductive success), a consequence that deserve closer investigation.…”

“…Although this is likely due to currency of benefits is easier to measure than the currency of costs, studies often also fail to consider them. For example, although obtaining EPP can increase the number of offspring for the males [44], seeking EPC also comes with search costs [41] and leaves the female unguarded in the same period, hence risking loss of within-pair paternity [45,46].…”

Divorce is linked with extra-pair paternity in a monogamous passerine

“…However extra-pair males, those from outside an established pair bond, can only provide indirect benefits to females. That is, extra-pair males may sire offspring without investing in costly parental care (Lebigre, Arcese, and Reid 2013;Raj Pant et al 2022; Table 1), the good genes hypothesis predicts that they should signal a better (Hamilton and Zuk 1982;Birkhead 1995;Kirkpatrick and Barton 1997), or more compatible (Blomqvist et al 2002;Ihle, Kempenaers, and Forstmeier 2015; but also see Griffith and Immler 2009) proposition than her social partner.…”