Data from: Detrimental effects of an autosomal selfish genetic element on sperm competitiveness in house mice

Female multiple mating (polyandry) is widespread across many animal taxa and indirect genetic benefits are a major evolutionary force favouring polyandry. An incentive for polyandry arises when multiple mating leads to sperm competition that disadvantages sperm from genetically inferior mates. A reduction in genetic quality is associated with costly selfish genetic elements (SGEs), and studies in invertebrates have shown that males bearing sex ratio distorting SGEs are worse sperm competitors than wild-type males. We used a vertebrate model species to test whether females can avoid an autosomal SGE, the t haplotype, through polyandry. The t haplotype in house mice exhibits strong drive in t heterozygous males by affecting spermatogenesis and is associated with homozygous in utero lethality. We used controlled matings to test the effect of the t haplotype on sperm competitiveness. Regardless of mating order, t heterozygous males sired only 11% of zygotes when competing against wild-type males, suggesting a very strong effect of the t haplotype on sperm quality. We provide, to our knowledge, the first substantial evidence that polyandry ameliorates the harmful effects of an autosomal SGE arising through genetic incompatibility. We discuss potential mechanisms in our study species and the broader implications for the benefits of polyandry.

雌性多次交配（polyandry，一妻多夫制）广泛存在于众多动物类群，间接遗传收益是推动一妻多夫制演化的主要进化动力。当多次交配引发精子竞争，使来自遗传劣质配偶的精子处于竞争劣势时，便会催生一妻多夫制的选择动因。遗传质量降低与代价高昂的自私遗传元件（selfish genetic elements, SGEs）密切相关，无脊椎动物相关研究已证实，携带性别比例扭曲型自私遗传元件的雄性，其精子竞争能力显著弱于野生型雄性。本研究以脊椎动物模式物种为实验对象，探究雌性是否可通过一妻多夫制规避常染色体自私遗传元件——t单倍型（t haplotype）。家鼠体内的t单倍型可通过干扰精子发生，在t杂合雄性中表现出强烈的驱动效应，且与纯合子宫内致死现象相关。我们通过受控交配实验，检验t单倍型对精子竞争能力的影响。结果显示，无论交配顺序如何，当与野生型雄性竞争时，t杂合雄性的子代仅占受精卵总数的11%，表明t单倍型对精子质量存在极强的负面影响。据我们所知，本研究首次提供了实质性证据，证明一妻多夫制能够缓解由遗传不相容性引发的常染色体自私遗传元件所带来的有害效应。最后，我们就该研究物种中的潜在作用机制，以及一妻多夫制演化收益的更广泛意义展开了讨论。