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.