Data from: Female ground tits prefer relatives as extra-pair partners: driven by kin-selection?

Socially monogamous female birds routinely mate with males outside the pair bond. Three alternative hypotheses consider genetic benefits as the major driver behind the female strategy. The inbreeding avoidance hypothesis predicts that females paired with closely related males should seek copulations with distantly related extra-pair partners to avoid fitness loss from inbreeding depression; the outbreeding avoidance hypothesis predicts the opposite; the kin-selection hypothesis suggests that regardless of social mate relatedness, females should give related males extra-pair fertilization opportunities to gain inclusive fitness if the costs from inbreeding are minor. We test these hypotheses with a facultative cooperative breeder, the ground tit (Parus humilis). Social pairs of ground tits formed randomly with respect to genetic relatedness. In both bi-parental and cooperative groups, a female’s engaging in extra-pair mating was independent of relatedness to her social mate; however, females preferred extra-pair sires to which they were more related than to their social mates. Moreover, females had higher relatedness with either their extra-group extra-pair sires in both bi-parental and cooperative groups, or within-group helper sires in cooperative groups, than expected by chance. When more than one potential extra-pair partner was available around a female’s nest, she tended to select a relative. There was no indication of fitness reduction from extra-pair mating, which occurred at an intermediate level of inbreeding. These data support the kin-selection hypothesis, although there might be alternative non-genetic reasons associated with the extra-pair mating preference. Our finding offers a new explanation for why female birds pursue extra-pair mating. It also may broaden our understanding of the role of kin-selection in the evolution of cooperative society.

实行社会一夫一妻制的雌性鸟类常会与配偶联结之外的雄性个体进行交配。现有三种备选假说，均将遗传收益视为雌性该繁殖策略的核心驱动因素。近交回避假说（inbreeding avoidance hypothesis）预测：与近缘雄性结成配偶的雌性，应选择与自身亲缘关系较远的婚外雄性进行交配，以规避近交衰退带来的适合度损失；远交回避假说（outbreeding avoidance hypothesis）则提出相反预测；亲缘选择假说（kin-selection hypothesis）指出：若近交带来的繁殖成本较低，那么无论其社会配偶的亲缘关系如何，雌性都应给予亲缘雄性婚外受精的机会，以此获得广义适合度（inclusive fitness）。我们以兼性合作繁殖者地山雀（Parus humilis）为研究材料，对上述三项假说开展检验。结果显示，地山雀的社会配偶配对与遗传亲缘关系并无关联。无论是双亲家庭还是合作繁殖群体中，雌性的婚外配行为均与其和社会配偶的亲缘关系无关；但相较于其社会配偶，雌性更倾向于选择亲缘关系更近的婚外父本（extra-pair sires）。此外，相较于随机预期水平，雌性与其群外婚外父本（无论是双亲家庭还是合作繁殖群体）、合作繁殖群体内的群内助手父本的亲缘关系均更高。当雌性巢穴周边存在多个潜在婚外配伴侣时，其往往会优先选择亲缘个体。本次研究未发现婚外配会导致适合度下降，且该类婚外配发生于中等程度的近交水平下。尽管雌性的婚外配偏好可能存在其他非遗传层面的解释，但本研究数据支持亲缘选择假说。我们的发现为雌性鸟类为何会进行婚外配提供了全新的解释视角，同时也有助于拓宽学界对亲缘选择在合作社会演化中所发挥作用的认知。