Data from: Genetic coupling of female mate choice with polygenic ecological divergence facilitates stickleback speciation

Ecological speciation with gene flow is widespread in nature, but it presents a conundrum: how are associations between traits under divergent natural selection and traits that contribute to assortative mating maintained? Theoretical models suggest that genetic mechanisms inhibiting free recombination between loci underlying these two types of traits (hereafter, “genetic coupling”) can facilitate speciation. Here, we perform a direct test for genetic coupling by mapping both divergent traits and female mate choice in a classic model of ecological speciation: sympatric benthic and limnetic threespine stickleback (Gasterosteus aculeatus). By measuring mate choice in F2 hybrid females, we allowed for recombination between loci underlying assortative mating and those under divergent ecological selection. In semi-natural mating arenas in which females had access to both benthic and limnetic males, we found that F2 females mated with males similar to themselves in body size and shape. In addition, we found two quantitative trait loci (QTLs) associated with female mate choice that also predicted female morphology along the benthic-limnetic trait axis. Furthermore, a polygenic genetic model that explains adaptation to contrasting benthic and limnetic feeding niches also predicted F2 female mate choice. Together, these results provide empirical evidence that genetic coupling of assortative mating with traits under divergent ecological selection helps maintain species in the face of gene flow, despite a polygenic basis for adaptation to divergent environments.

存在基因流的生态物种形成在自然界中广泛分布，但这一现象却存在一个难解谜题：受歧化自然选择作用的性状，与参与选型交配的性状之间的关联，究竟是如何得以维持的？理论模型显示，能够抑制这两类性状所在基因座间自由重组的遗传机制（下称“遗传耦合（genetic coupling）”），可促进物种形成。本研究以生态物种形成的经典研究模型——同域底栖型与浮游型三棘刺鱼（Gasterosteus aculeatus）为对象，通过定位歧化性状与雌性择偶偏好，对遗传耦合效应开展了直接检验。我们通过测定F2杂交雌性个体的择偶行为，使得参与选型交配的基因座与受歧化生态选择的基因座之间得以发生重组。在雌性可同时接触底栖型与浮游型雄性的半自然交配竞技场中，实验结果表明，F2雌性更倾向于选择体型与自身形态相似的雄性。此外，我们鉴定到两个与雌性择偶偏好相关的数量性状基因座（QTLs），这些基因座同时能够预测雌性在底栖-浮游性状轴上的形态特征。进一步分析显示，能够解释对底栖与浮游型取食生态位适应性分化的多基因遗传模型，同样可以预测F2雌性的择偶偏好。综上，本研究提供了实验证据，表明选型交配与受歧化生态选择的性状间的遗传耦合，能够在基因流存在的条件下维持物种分化，即便适应歧化环境的遗传基础为多基因调控。