Hybridization underlies localized trait evolution in cavefish

A rapidly growing body of work has demonstrated that introgressive hybridization often drives patterns of phenotypic evolution and may play an integral role in the evolutionary processes of local adaptation and speciation. Indeed, several of studies have shown that behavioral variation can result from introgressive hybridization (e.g., song in hybrid Darwin's finches, mate choice in hybrid baboons, defensive behavior in hybrid honey bees), providing new substrate for selection to act upon. A powerful model system for investigating the genetic and evolutionary basis of trait development and behavior is the Mexican tetra, Astyanax mexicanus. Cave populations have repeatedly evolved numerous traits including eye loss, sleep loss, and albinism. Of the 30 caves inhabited by A. mexicanus, the Chica cave is unique because it contains several pool microenvironments inhabited by putative hybrids between surface and cave populations, providing an opportunity to investigate hybridization and its impact on complex trait evolution. We demonstrate that hybridization between cave and surface populations contributes to highly localized variation in pigmentation, eye development, and sleep, traits that are thought to be associated with cave evolution. Our findings suggest that hybridization drives highly-localized behavioral and morphological evolution. Lastly, our analyses uncovered a compelling example of convergent evolution in a core circadian clock gene in multiple independent cavefish lineages and burrowing mammals, suggesting a shared genetic mechanism underlying circadian disruption in subterranean vertebrates. Together, our results provide insight into the evolutionary mechanisms that generate adaptive genetic variation.日益增多的研究成果表明，渐渗杂交（introgressive hybridization）常塑造表型进化（phenotypic evolution）模式，并可能在本地适应（local adaptation）与物种形成（speciation）等进化过程中发挥不可或缺的作用。已有多项研究证实，行为变异（behavioral variation）可由渐渗杂交引发——例如达尔文地雀杂交后代的鸣唱、狒狒杂交个体的配偶选择，以及杂交蜜蜂的防御行为，这为自然选择提供了新的作用底物。用于探究性状发育（trait development）与行为的遗传及进化基础的经典模型系统之一，是墨西哥丽脂鲤（Astyanax mexicanus）。该物种的洞穴种群反复演化出诸多特征，包括眼部退化、睡眠缺失与白化症（albinism）。在墨西哥丽脂鲤栖息的30处洞穴中，奇卡洞穴（Chica cave）独具特色：其内部存在多个水池微生境（pool microenvironments），栖息着地表种群与洞穴种群的疑似杂交个体（putative hybrids），为研究渐渗杂交及其对复杂性状进化的影响提供了绝佳契机。本研究证实，洞穴种群与地表种群间的杂交，会导致色素沉着（pigmentation）、眼部发育（eye development）及睡眠等性状出现高度局域化的变异，而这些性状通常被认为与洞穴适应性演化密切相关。研究结果表明，渐渗杂交可驱动高度局域化的行为与形态演化。此外，本研究还在多个独立的洞穴鱼谱系与穴居哺乳动物中，发现了生物钟核心基因（circadian clock gene）的趋同进化（convergent evolution）实例，暗示地下脊椎动物（subterranean vertebrates）的生物钟紊乱可能共享同一套遗传机制。综上，本研究结果为解析产生适应性遗传变异的进化机制提供了新的认知。