Extreme polyandry aids the establishment of invasive populations of a social insect

Although monandry is believed to have facilitated the evolution of eusociality, many highly eusocial insects have since evolved extreme polyandry. The transition to extreme polyandry was likely driven by the benefits of within-colony genetic variance to task specialization and/or disease resistance, but the extent to which it confers secondary benefits, once evolved, is unclear. Here we investigate the consequences of extreme polyandry on the invasive potential of the Asian honey bee, Apis cerana. In honey bees and other Hymenoptera, small newly founded invasive populations must overcome the genetic constraint of their sex determination system that requires heterozygosity at a sex-determining locus to produce viable females. We find A. cerana queens in an invasive population mate with an average of 27 males (range 16–42) that would result in the founding queen/s carrying 75% of their source population’s sex alleles in stored sperm. This mating frequency is similar to native-range Chinese A. cerana (mean 29 males, range 19–46). Simulations reveal that extreme polyandry reduces the risk, relative to monandry or moderate polyandry, that colonies produce a high incidence of inviable brood in populations that have experienced a founder event, that is, when sex allele diversity is low and/or allele frequencies are unequal. Thus, extreme polyandry aids the invasiveness of A. cerana in two ways: (1) by increasing the sex locus allelic richness carried to new populations with each founder, thereby increasing sex locus heterozygosity; and (2) by reducing the population variance in colony fitness following a founder event.

尽管学界普遍认为单雄交配（monandry）曾推动真社会性（eusociality）的演化，但诸多高度真社会性昆虫后续却演化出了极端多雄交配策略。极端多雄交配的演化转变，大概率源于蜂群内遗传变异对劳动分工与/或抗病性的益处；但该策略演化成型后所能带来的次生益处究竟几何，目前仍不明确。本研究针对极端多雄交配对东方蜜蜂（Apis cerana）入侵潜力的影响展开探究。在蜜蜂及其他膜翅目（Hymenoptera）昆虫中，新近建立的小型入侵种群必须克服其性别决定系统的遗传限制：该系统要求性别决定位点（sex-determining locus）处于杂合状态，才能产生可存活的雌性个体。我们发现，某入侵种群中的东方蜜蜂蜂王，平均与27只雄蜂交配（交配范围为16至42只），该交配模式可使创始蜂王通过储存的精子，携带其源种群75%的性等位基因。该交配频率与中国本土的东方蜜蜂种群相近（平均29只雄蜂，交配范围为19至46只）。模拟实验结果显示：相较于单雄交配或中度多雄交配，极端多雄交配可降低种群在经历奠基者事件（founder event）后，蜂群产生高比例不育幼虫的风险——此类事件发生时，性等位基因多样性较低且/或等位基因频率分布不均。综上，极端多雄交配通过两种途径助力东方蜜蜂的入侵能力：其一，提升每个创始个体携带至新种群的性别位点等位基因丰富度，进而提高性别位点的杂合度；其二，降低奠基者事件后蜂群适合度的种群方差。