Genetic monogamy despite frequent extrapair copulations in “strictly monogamous” wild jackdaws

“Monogamy” refers to different components of pair exclusiveness: the social pair, sexual partners, and the genetic outcome of sexual encounters. Avian monogamy is usually defined socially or genetically, whereas quantifications of sexual behavior remain scarce. Jackdaws (Corvus monedula) are considered a rare example of strict monogamy in songbirds, with lifelong pair bonds and little genetic evidence for extrapair (EP) offspring. Yet jackdaw copulations, although accompanied by loud copulation calls, are rarely observed because they occur visually concealed inside nest cavities. Using full-day nest-box video surveillance and on-bird acoustic bio-logging, we directly observed jackdaw sexual behavior and compared it to the corresponding genetic outcome obtained via molecular parentage analysis. In the video-observed nests, we found genetic monogamy but frequently detected forced EP sexual behavior, accompanied by characteristic male copulation calls. We, thus, challenge the long-held notion of strict jackdaw monogamy at the sexual level. Our data suggest that male mate guarding and frequent intrapair copulations during the female fertile phase, as well as the forced nature of the copulations, could explain the absence of EP offspring. Because EP copulation behavior appeared to be costly for both sexes, we suggest that immediate fitness benefits are an unlikely explanation for its prevalence. Instead, sexual conflict and dominance effects could interact to shape the spatiotemporal pattern of EP sexual behavior in this species. Our results call for larger-scale investigations of jackdaw sexual behavior and parentage and highlight the importance of combining social, sexual, and genetic data sets for a more complete understanding of mating systems. Lay Summary Monogamy is defined at the social, sexual, and genetic levels—which do not necessarily match. Based on genetic findings, jackdaws are considered a rare example of avian monogamy. In a colony of wild jackdaws, we found that extrapair (EP) copulations occurred frequently but without yielding EP offspring. This behavior was seemingly male driven and forced and prevented by mate guarding during female fertility. Our results highlight the importance of combining genetics and behavior to better understand mating systems.