Montgomery Stephen H, Rossi Matteo, McMillan W Owen, Merrill Richard M
School of Biological Science, University of Bristol, Bristol BS8 1TQ, United Kingdom;
Smithsonian Tropical Research Institute, 0843-03092 Gamboa, Panama.
Proc Natl Acad Sci U S A. 2021 Feb 9;118(6). doi: 10.1073/pnas.2015102118.
The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, butterflies. Despite ongoing gene flow, sympatric species pairs within the complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that and clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first-generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation.
行为进化在物种形成过程中的重要性已得到充分确立，但我们对其在感觉和神经系统中的表现却知之甚少。一些研究已将特定的神经变化与物种形成过程中宿主或配偶偏好的差异联系起来。然而，大脑适应当地环境条件的程度，以及这是否有助于在生态上已经分化的近亲之间形成生殖隔离，仍然未知。在这里，我们研究了亲缘关系密切但生态特征不同的蝴蝶之间大脑形态和神经基因表达的差异。尽管存在基因流动，但该复合体中的同域物种对在从开阔森林到封闭森林以及光照强度降低的梯度上始终保持分离。通过为107只蝴蝶生成定量神经解剖学数据，我们表明 和 分支在其地理范围内大脑形态有显著变化，不同的结构集中在视觉系统中。这些神经解剖学差异在神经基因表达的广泛差异中得到反映。神经形态和基因表达的差异都是可遗传的，超过了中性分化的预期速率，并在第一代杂交后代中产生中间性状。强烈的分歧选择证据表明，在每个亲本微生境中局部适应不同的选择最优值，这表明杂种的中间性状与任何一种条件都不太匹配。因此，神经特征可能有助于同时形成基因流动障碍，从而有助于促进物种形成。
