Data from: Increased male investment in sperm competition results in offspring of lower quality

Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male-bias is that competition over fertilization of female gametes leads to sexual selection for increased male germline replication at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here we test this hypothesis using experimental evolution lines of the seed beetle Callosobruchus maculatus, maintained for >50 generations under three alternative mating regimes: natural and sexual selection (N+S-lines), natural selection only (N-lines) or sexual selection only (S-lines). Previous findings suggest that S-males reduce germline maintenance when engaging in reproduction compared to N- and N+S-males. Here, we first show that S-males are superior in sperm competition compared to both N- and N+S-males, suggesting that the removal of trade-offs between naturally and sexually selected male fitness components has resulted in the evolution of increased post-copulatory reproductive success. We then show that S-males produce progeny of lower quality if engaging in socio-sexual interactions with conspecifics prior to being challenged with a dose of irradiation introducing DNA-damage in their germline. We identify 18 candidate genes that showed differential expression in response to the induced germline damage. These genes also showed significant expression changes across socio-sexual treatments of fathers and predicted the reduction in quality of their offspring. Moreover, sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. Our findings provide evidence for a trade-off between male success in sperm competition and germline maintenance, suggesting that sex-differences in the relative strengths of sexual and natural selection are causally linked to male-mutation bias.雄性动物通常相较于同种雌性个体展现出更高的突变率。针对这一雄性偏倚现象的假说认为，雌性配子受精竞争会引发性选择，使得雄性生殖系复制增多，却以维持与修复能力为代价，进而在精子竞争中的雄性成功率与后代质量之间形成权衡。本研究以绿豆象（Callosobruchus maculatus）的实验进化品系为材料，在三种不同交配制度下持续培养超过50个世代：自然选择与性选择共存组（N+S组）、仅自然选择组（N组），以及仅性选择组（S组）。已有研究表明，相较于N组与N+S组的雄性，S组雄性在繁殖过程中会降低生殖系维持能力。本研究首先证实，相较于N组与N+S组雄性，S组雄性在精子竞争中表现更优异，这提示移除自然选择与性选择所对应的雄性适合度组分间的权衡，可演化出更高的交配后生殖成功率。随后我们发现，若S组雄性在接受引入生殖系DNA损伤的辐照处理前，先与同种个体进行社会性互动，则其产生的后代质量更低。我们共鉴定出18个候选基因，这些基因在诱导产生的生殖系损伤响应中呈现差异表达。这些基因在父亲的社会性互动处理间同样存在显著表达变化，且可预测其后代的质量下降。此外，这18个基因的表达存在性别差异，表明雌性在生殖系维持上的投入显著更高。我们的研究结果为精子竞争成功率与生殖系维持之间的权衡提供了证据，提示性选择与自然选择相对强度的性别差异，与雄性突变偏倚存在因果关联。