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（gene flow）的生态物种形成（ecological speciation）在自然界中广泛分布，但该现象却存在一个核心悖论：受趋异自然选择（divergent natural selection）作用的性状，与参与选型交配（assortative mating）的性状之间的关联，究竟如何得以维持？理论模型指出，能够抑制这两类性状所在基因座间自由重组的遗传机制（genetic coupling，下文简称“遗传耦合”），可有效促进物种形成过程。本研究以经典生态物种形成模型——同域底栖与浮游型三刺棘鱼（Gasterosteus aculeatus）为研究体系，通过对趋异性状与雌性择偶偏好开展遗传定位，直接检验了遗传耦合假说。我们通过对F2代杂交雌性个体开展择偶实验，使得参与选型交配的基因座与受趋异生态选择作用的基因座之间能够发生重组。在可供雌性个体同时接触底栖型与浮游型雄性的半自然交配竞技场中，我们发现F2代杂交雌性更倾向于与自身体型与形态特征相似的雄性完成交配。此外，我们鉴定出两个与雌性择偶偏好相关的数量性状位点（quantitative trait loci, QTLs），这些位点同时可以预测雌性在底栖-浮游形态轴上的表型特征。进一步分析显示，能够解释对底栖与浮游型不同觅食生态位（feeding niches）适应的多基因遗传模型，同样可以有效预测F2代杂交雌性的择偶偏好。综上，本研究的实验结果提供了实证证据：尽管适应趋异环境的遗传基础为多基因架构，但选型交配与受趋异生态选择作用的性状之间的遗传耦合，能够在基因流存在的条件下，帮助维持物种的独立性。