Why inclusive fitness can make it adaptive to produce less fit extra-pair offspring

Abstract

Social monogamy predominates in avian breeding systems, but most socially monogamous species engage in promiscuous extra-pair copulations (EPCs). The reasons behind this remain debated, and recent empirical work has uncovered patterns that do not seem to fit existing hypotheses. In particular, some results seem to contradict the inbreeding avoidance hypothesis: females can prefer extra-pair partners that are more closely related to them than their social partners, and extra-pair young can have lower fitness than within-pair young. Motivated by these studies, we show that such results can become explicable when an asymmetry in inbreeding tolerance between monogamy and polygamy is extended to species that combine both strategies within a single reproductive season. Under fairly general conditions, it can be adaptive for a female to choose an unrelated social partner, but inbreed with an extrapair partner. Inbreeding depression is compensated for by inclusive fitness benefits, which are only fully realized in EPCs. We also show that if a female has already formed a suboptimal social bond, there are scenarios where it is beneficial to engage in EPCs with less related males, and others where EPCs with more related males increase her inclusive fitness. This has implications for detecting general relatedness or fitness trends when averaged over several species.

Predictably Philandering Females Prompt Poor Paternal Provisioning

“…Our results warrant more research into these interacting effects between female and male behavior in a pair. Such interacting within-male effects between mating partners are likely to be frequent and have the power to challenge our traditional models about sexual conflict, mate choice, and parental care (Westneat and Stewart 2003;Alonzo 2010;Lehtonen and Kokko 2015) but have not often been investigated (Alonzo and Heckman 2009).…”

Inbreeding risk, avoidance and costs in a group-living primate, Cebus capucinus

“…However, models based on evolutionary theory also predict that there is an optimal degree of similarity between parents that helps keep co-adapted genes in a population together ('optimal outbreeding', Bateson 1983), and that some degree of inbreeding should be allowed or tolerated when the inclusive fitness benefits of mating with kin or the costs of finding alternative mates outweigh any potential costs to infant fitness (Parker 1979;Smith 1979;Waser et al 1986;Lehmann and Perrin 2003;Kokko and Ots 2006;Jamieson et al 2009;Puurtinen 2011;Lehtonen and Kokko 2015). Thus, evolutionary theory can also predict a tolerance for, or even a preference for, some forms of kin as mating partners.…”

Apparent inbreeding preference despite inbreeding depression in the American crow

“…Even if a lower percentage of inbred offspring survive (Townsend, Clark, McGowan, Buckles et al., ; this study; Townsend, Clark, McGowan, Miller et al., ), those that do survive will carry more alleles that are identical to the parents’ alleles than outbred offspring, which can—under certain conditions (Puurtinen, ; Reid, Arcese, Bocedi et al., ; Waser, Austad, & Keane, )—offset the losses of inbreeding depression. Both males and females are expected to be particularly tolerant of inbreeding (below some threshold value of inbreeding depression) if it does not come at a cost of reproductive opportunities for the mate‐limited sex (Lehtonen & Kokko, ; Waser et al., ). Inbreeding tolerance might be higher when it occurs through extra‐pair matings, for example, if these lead to reproductive output that a male relative would not otherwise obtain.…”