Data from: Meiotic drive changes sperm precedence patterns in house mice: potential for male alternative mating tactics

Background - With female multiple mating (polyandry), male-male competition extends to after copulation (sperm competition). Males respond to this selective pressure through physiological, morphological and behavioural adaptations. Sperm competitiveness is commonly decreased in heterozygote carriers of male meiotic drivers, selfish genetic elements that manipulate the production of gametes in males. This might give carriers an evolutionary incentive to reduce the risk of sperm competition. Here, we explore this possibility in house mice. Natural populations frequently harbour a well-characterised male driver (t haplotype), which is transmitted to 90% of heterozygous (+/t) males' offspring. Previous research demonstrated strong detrimental effects on sperm competitiveness, and suggested that +/t males are particularly disadvantaged against wild type males when first-to-mate. Low paternity success in the first-to-mate role is expected to favour male adaptations that decrease the risk of sperm competition by preventing female remating. Genotype-specific paternity patterns (sperm precedence) could lead to genetically determined alternative reproductive tactics that can spread through gene level selection. Here, we seek confirmation that +/t males are generally disadvantaged when first-to-mate and address whether males of different genotypes differ in reproductive tactics (copulatory and morphological) to maximise individual or driver fitness. Finally, we attempt to explain the mechanistic basis for alternative sperm precedence patterns in this species. Results - We confirmed that +/t males are weak sperm competitors when first to mate. When two +/t males competed, the second-to-mate was more successful, which contrasts with first male sperm precedence when wild type males competed. However, we found no differences between male genotypes in reproductive behaviour or morphology that were consistent with alternative reproductive tactics. Sperm of +/+ and +/t males differed with respect to in vitro sperm features. Premature hypermotility in +/t males' sperm can potentially explain why +/t males are very weak sperm competitors when first-to-mate. Conclusions - Our results demonstrate that meiotic drivers can have strong effects on sperm precedence patterns, and may provide a heritable basis for alternative reproductive tactics motivated by reduced sperm competitiveness. We discuss how experimental and evolutionary constraints may help explain why male genotypes did not show the predicted differences.研究背景——在雌性多配（polyandry，即一妻多夫制）的物种中，雄性间的竞争会延伸至交配后阶段，即精子竞争。雄性会通过生理、形态及行为层面的适应来应对这一选择压力。雄性减数分裂驱动因子（male meiotic drivers）是一类可操控雄性配子产生过程的自私遗传元件（selfish genetic elements），其杂合携带者的精子竞争力通常会出现下降。这一现象可能会为携带者带来降低精子竞争风险的进化动力。本研究以家鼠为研究对象，对此展开探讨。 自然种群中普遍存在一种特征明确的雄性驱动因子——t单倍型（t haplotype），该因子可传递给90%的杂合（+/t）雄性后代。既往研究已证实其对精子竞争力存在显著的负面影响，并提出当+/t雄性作为首个交配者时，其相较于野生型雄性会处于明显的竞争劣势。首个交配者的父权成功率较低的情况，会促使雄性演化出通过阻止雌性再次交配来降低精子竞争风险的适应策略。基因型特异性的父权模式（精子优先性，sperm precedence）可能会催生由遗传决定的替代生殖策略，并可通过基因层面的选择进行传播。 本研究旨在确认+/t雄性在作为首个交配者时普遍处于竞争劣势这一结论，并探究不同基因型雄性是否会在生殖策略（包括交配行为与形态特征）上存在差异，以最大化个体自身或驱动因子的适合度。最后，本研究尝试阐释该物种中替代精子优先性模式的机制基础。 研究结果——本研究证实，当作为首个交配者时，+/t雄性确实属于弱势精子竞争者。当两只+/t雄性发生精子竞争时，第二个交配的雄性会获得更高的父权成功率，这与野生型雄性竞争时出现的首个雄性精子优先模式截然相反。然而，本研究未发现不同基因型雄性在生殖行为或形态特征上存在与替代生殖策略相符的差异。 体外实验显示，+/+与+/t雄性的精子在多项体外精子特征上存在差异。+/t雄性精子出现的过早超活化现象，或可解释为何当其作为首个交配者时，精子竞争力会显著低下。 研究结论——本研究结果表明，减数分裂驱动因子可对精子优先模式产生显著影响，并可能为因精子竞争力下降而催生的替代生殖策略提供可遗传的基础。本研究还讨论了实验约束与进化约束如何帮助解释为何不同基因型雄性未表现出预期的策略差异。