Indirect genetic effects improve female extra-pair heritability estimates

Abstract

The question of why females engage in extra-pair behaviours is long-standing in evolutionary biology. One suggestion is that these behaviors are maintained through pleiotropic effects on male extra-pair behaviors and lifetime reproductive success (genes controlling extra-pair behaviours are shared between sexes, but only beneficial to one, in this case, males). However, for this to occur extra-pair behaviour must be heritable and positively genetically correlated between sexes. Although previous studies have suggested low heritability with no evidence for between-sex genetic correlations in extra-pair behaviours, indirect genetic effects (those derived from the behaviour of others, IGEs) from the social partner, the influence of the social partners genotype on the phenotype of an individual, have not been considered, despite the potential to uncover hidden heritability. Using data from a closed house sparrow population with a genetic pedigree spanning two decades, we tested the influence of IGEs on heritability and genetic correlation estimates of extra-pair behaviour. We found that the inclusion of IGEs improved model fit for both male and female extra-pair heritability. While IGEs did not change between-sex genetic correlations, we found a reduction in uncertainty in our estimates. Future studies should consider the effect of IGEs on the mechanisms of sex specific extra-pair behaviour.

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

“…(Reid et al 2011;Grinkov et al 2020). However, Dobson et al. (2023) found that the inclusion of social partner indirect genetic effects (those derived from the behaviour of another) improved model fit for the heritability of both male and female extra-pair behaviour, implying a role for the wider social environment in the plasticity of extra-pair behaviour.…”

“…Although we consider our data to be near-complete, our phenotypic study is still subject to some bias (Hadfield 2008). For example, we sampled chicks for paternity at day two, (see Dunning et al 2023), but this may still exclude an invisible fraction of those pairs, females (Kidd et al 2015) or eggs (Yuta et al 2018;Assersohn et al 2021) who fail early. As a result, our study measures extra-pair paternity, and not extra-pair copulations, which could be more frequent than is reflected in paternity analysis (Fossøy, Johnsen, and Lifjeld 2006;Girndt 2018).…”

“…The social environment may be another mediator of extra-pair behaviour (Maldonado-Chaparro et al 2018; Table 1), where individuals with high sociality -their propensity to associate with others -likely have more opportunity to choose partners from larger pools of potential mates. Accordingly, the number (Oh and Badyaev 2010;Dunning et al 2023) and quality (Firth and Sheldon 2016;Beck, Farine, and Kempenaers 2021) of social associations were empirically shown to be linked to reproductive success, including extra-pair mate choice (Beck, Farine, and Kempenaers 2020). Empirical studies generally find that extra-pair partners are more likely to be close neighbours (Westneat and Sherman 1997;Schlicht, Valcu, and Kempenaers 2015;Mingju et al 2017;Beck, Farine, and Kempenaers 2020;Beck, Valcu, and Kempenaers 2020), adding weight to the role of opportunism in extra-pair copulation (as empirically demonstrated by Fossøy, Johnsen, and Lifjeld 2006;and theoretically by Brommer et al 2007;.…”

“…found no relationship between genes beneficial to male reproductive success and female extra-pair behaviour (an example of intersexual antagonistic pleiotropy). Further, quantitative approaches to understanding pleiotropic effects on female extra-pair behaviours have resulted in inconclusive effect sizes, for two reasons: First, the heritability of male and female promiscuity is closely related to fitness, masking any evidence of pleiotropy effect (Reid et al 2011;Reid 2015;Dobson et al 2023); And second, studies with genetic pedigrees from wild populations are scarce and have few generations, resulting in inconclusive effect sizes (Reid et al 2011;Moiron, Charmantier, and Bouwhuis 2022;Dobson et al 2023), even where prevalence of extra-pair behaviour is high. However, if pleiotropic effects are driving female extra-pair behaviour, then the expression of two linked behaviours should be empirical -if not genetically -detectable in wild systems.…”

“…Hypotheses referenced in this manuscript, seeBrouwer and Griffith (2019) for a comprehensive review Schroeder et al 2012;Dunning et al 2023)…”