Department of Ecology and Genetics, Animal Ecology, Uppsala University, Uppsala, Sweden.
Department of Zoology, Animal Ecology, Martin-Luther University Halle-Wittenberg, Halle (Saale), Germany.
PLoS Biol. 2023 Apr 4;21(4):e3002049. doi: 10.1371/journal.pbio.3002049. eCollection 2023 Apr.
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 increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus. We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection, resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in sociosexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across sociosexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance. While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the allocation decisions of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.
雄性动物的突变率通常高于其雌性同类。对于这种雄性偏向的一个假设是，对雌性配子受精的竞争导致雄性在繁殖上的投入增加，而牺牲了维持和修复，从而在精子竞争中的雄性成功和后代质量之间产生了权衡。在这里，我们通过利用实验进化的力量来研究性选择对种子象鼻虫 Callosobruchus maculatus 雄性生殖系的影响，为这一假设提供了证据。我们首先表明，在强烈的性选择下经过 50 代的进化，加上对自然选择的实验去除，导致雄性在精子竞争中更成功。然后我们表明，如果雄性在被挑战监视和修复其生殖系中实验诱导的损伤之前进行社交互动，它们会产生后代质量较低的后代，而仅仅存在雄性竞争对手就足以引起这种反应。我们鉴定了 18 个候选基因，这些基因对诱导的生殖系损伤表现出差异表达，其中一些先前与 DNA 修复和细胞维持过程有关。这些基因在父亲的社交处理中也表现出显著的表达变化，并预测了它们后代质量的降低，其中一个基因的表达也与雄性精子竞争的成功密切相关。同一 18 个基因的性别差异表达表明雌性在生殖系维持方面的投资大大增加。虽然需要做更多的工作来详细说明我们结果的确切分子基础，但我们的发现为精子竞争成功和生殖系维持之间的权衡提供了罕见的实验证据。这表明，性选择和自然选择的相对强度的性别差异与雄性突变偏向因果相关。这里提倡的原则是，个体的分配决策可以影响其生殖系的可塑性及其后代的遗传质量，这对配偶选择过程有几个有趣的影响。
