Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, PA 16802, USA.
Department of Integrative Biology, Michigan State University, East Lansing, MI 48824, USA.
Proc Biol Sci. 2024 Jul;291(2027):20240121. doi: 10.1098/rspb.2024.0121. Epub 2024 Jul 31.
Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Stickleback fish differentially adapted to limnetic and benthic habitats are reproductively isolated and females of each species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioural data from a mate choice experiment with gene expression profiles from the brains of females actively deciding whether to mate. We find substantial gene expression variation between limnetic and benthic females, regardless of behavioural context, suggesting general divergence in constitutive gene expression patterns, corresponding to their genetic differentiation. Intriguingly, female gene co-expression modules covary with male display traits but in opposing directions for sympatric populations of the two species, suggesting male displays elicit a dynamic neurogenomic response that reflects known differences in female preferences. Furthermore, we confirm the role of numerous candidate genes previously implicated in female mate choice in other species, suggesting evolutionary tinkering with these conserved molecular processes to generate divergent mate preferences. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making critical for generating sexual isolation and speciation.
配偶选择在物种形成中起着至关重要的作用，但我们对支持这一关键决策过程的分子机制知之甚少。适应于淡水和底栖生境的刺鱼是生殖隔离的，并且每种鱼的雌性都使用不同的雄性特征来评估潜在的配偶，并拒绝异源雄性。在这里，我们将来自配偶选择实验的行为数据与来自主动决定是否交配的雌性大脑的基因表达谱相结合。我们发现，无论行为背景如何，淡水和底栖雌性之间都存在大量的基因表达差异，这表明它们的遗传分化导致了组成型基因表达模式的普遍分歧。有趣的是，雌性基因共表达模块与雄性展示特征相关，但对于两个物种的同域种群来说，其方向相反，这表明雄性展示引发了一种反映雌性偏好差异的动态神经基因组反应。此外，我们还证实了许多先前在其他物种的雌性配偶选择中涉及的候选基因的作用，这表明这些保守的分子过程发生了进化性的调整，以产生不同的配偶偏好。总之，我们的研究为理解女性决策背后的分子过程提供了重要的新见解，这些过程对于产生性隔离和物种形成至关重要。
