Genetic benefits of female from extra-pair paternity are context dependent within the socially monogamous Tree Sparrow

Females actively seek extra-pair paternity (EPP) to acquire a fitness advantage for their offspring. The “context-dependence hypothesis” posits that female extra-pair mate choice has plasticity in response to environmental conditions, and therefore magnitude of female genetic benefits from EPP depends on the environmental variation. Furthermore, chronic heavy metal pollution can cause adverse effects on fitness-related traits of wild birds. However, few studies were available on the interactions between heavy metal pollution and EPP. We selected an area that was contaminated by heavy metals for more than 60 years (Baiyin, BY), a relatively unpolluted area (Liujiaxia, LJX), and Tree Sparrows (Passer montanus) as study species to explore the response of female extra-pair mate choice and genetic benefits from EPP to heavy metal pollution in socially monogamous birds. The relatedness between social mates and extra-pair mates was investigated. Additionally, we compared the body size and heterozygosity of extra-pair offspring (EPO), within-pair offspring (WPO), social males and extra-pair males from the two Tree Sparrow populations. We found that at BY, female Tree Sparrows tended to choose extra-pair males with larger body size and lower genetic similarity, thereby producing higher heterozygosity and larger body size of EPO compared with those of WPO. However, no similar phenomenon was observed in the Tree Sparrow population from LJX. In addition, there was a significant interaction between population and paternity in the analyses of the fitness-related traits, suggesting that environmental variation could affect female genetic benefits from EPP. This study confirmed the existence of presumed interactions between environmental pollution and EPP within the natural population of socially monogamous Tree Sparrows. Our findings shed lights on the possible effects of long-term environmental stress on mating system in wild birds.