Extra-pair mating and evolution of cooperative neighbourhoods

A striking but unexplained pattern in biology is the promiscuous mating behaviour in socially monogamous species. Although females commonly solicit extra-pair copulations, the adaptive reason has remained elusive. We use evolutionary modelling of breeding ecology to show that females benefit because extra-pair paternity incentivizes males to shift focus from a single brood towards the entire neighbourhood, as they are likely to have offspring there. Male-male cooperation towards public goods and dear enemy effects of reduced territorial aggression evolve from selfish interests, and lead to safer and more productive neighbourhoods. The mechanism provides adaptive explanations for the common empirical observations that females engage in extra-pair copulations, that neighbours dominate as extra-pair sires, and that extra-pair mating correlates with predation mortality and breeding density. The models predict cooperative behaviours at breeding sites where males cooperate more towards public goods than females. Where maternity certainty makes females care for offspring at home, paternity uncertainty and a potential for offspring in several broods make males invest in communal benefits and public goods. The models further predict that benefits of extra-pair mating affect whole nests or neighbourhoods, and that cuckolding males are often cuckolded themselves. Derived from ecological mechanisms, these new perspectives point towards the evolution of sociality in birds, with relevance also for mammals and primates including humans

Multimodal flight display of a neotropical songbird predicts social pairing but not extrapair mating success

Models of sexual selection predict that socially monogamous females may gain direct or indirect (genetic) benefits by mating with multiple males. We addressed current hypotheses by investigating how, in the socially monogamous blue-black grassquit (Volatinia jacarina), male courtship and territory quality varied with social and extrapair paternity. Males of this tropical granivorous passerine exhibit multimodal displays integrating motor (leap displays) and acoustic components. Across 3 years, we found that extrapair paternity ranged from 8 to 34 % of all nestlings and from 11 to 47 % of all broods. Extrapair and socially paired male territories had similar seed densities. Females preferred to pair socially with males executing higher leaps, but no other male display characteristic associated with paternity loss and extrapair fertilizations. Extrapair and social mates did not differ in genetic similarity to female partners nor in inbreeding levels. Additionally, inbreeding and body condition of extrapair and within-pair nestlings did not differ. Thus, not only did we reject the direct benefits hypothesis for extrapair copulations, but our results also did not support the additive and nonadditive genetic benefits hypotheses. Instead, we found support for benefits through selection of potentially “good fathers,” specifically for females that chose to pair socially with males exhibiting enhanced performance in their displays.</p