Patterns of paternity skew among polyandrous social insects: What can they tell us about the potential for sexual selection?

Monogamy results in high genetic relatedness among offspring and thus it is generally assumed to be favoured by kin selection. Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females. We performed a large scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness amongst colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized amongst potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for post-copulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.

单配偶制可使后代间维持较高的遗传相关性（genetic relatedness），因此通常被认为是受亲缘选择（kin selection）青睐的繁殖模式。然而，一妻多夫制（polyandry，即雌性多次交配）在社会膜翅目（social Hymenoptera，蚂蚁、蜜蜂与胡蜂）中已独立演化多次，学界已开展大量研究以探究其演化代价与适应收益。不过，遗传相关性与广义适合度收益不仅受蜂王交配频次的影响，还受父权偏斜（paternity skew）的调控——父权偏斜是量化衡量一妻多夫雌性后代间父系分配偏倚程度的指标。本研究针对一妻多夫的社会膜翅目类群，开展了跨物种的大规模系统发育分析。研究发现，交配频次与父权偏斜之间普遍存在显著的负相关关系。在交配频次较低的类群中，父权偏斜程度较高——这种偏斜会提升蜂群成员间的遗传相关性，进而最大化广义适合度收益。而蜂王交配频次极高的类群则呈现较低的父权偏斜，其潜在父本间的后代分配比例趋于均等。父本间的均等后代分配，可最大化由后代遗传多样性带来的适应收益。本研究探讨了交配后性选择对社会昆虫父系分配模式的潜在影响，并提出性选择或许在社会演化中发挥了关键却长期被忽视的作用。