A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh,cfap20,rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5,ext1,cyp26b1,galr2), and finally the only de novo non-synonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a new framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

为探究脊椎动物适应性辐射（vertebrate adaptive radiation）的起源与演化阶段，我们基于202尾加勒比鳉鱼的基因组数据，重建了驱动主要分化表型轴的适应性等位基因的时空演化历史。在一座巴哈马岛屿上，源自不同地理来源的古老现存遗传变异，在针对食鳞与食软体动物这两类新兴营养生态位的强定向选择作用下，被重新组合为全新的基因型组合。我们的研究为适应性辐射的两大长期存在的假说提供了证据：杂交群起源假说与适应性演化的时间阶段假说。结合群体基因组学、转录组学与全基因组关联分析（genome-wide association mapping）技术手段，我们证实，位于巴哈马圣萨尔瓦多岛的这一微特有营养生态位特化种适应性辐射，其适应性基因渐渗（adaptive introgression）水平是邻近岛屿广食性种群的两倍，且适应性分化呈现阶段性特征：首先，与摄食行为相关的基因（prlh、cfap20、rmi1）的现存调控变异被选择固定；其次，与颅面部及肌肉发育相关的基因（itga5、ext1、cyp26b1、galr2）的现存调控变异被固定；最后，成骨转录因子与癌基因twist1上仅有的新生非同义替换最晚被选择固定。我们的研究结果表明，储存在不同环境避难所中的古老等位基因，可被组装为全新的适应性组合，同时也为重建适应性演化与物种形成（speciation）的时空格局提供了全新的研究框架。