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 the 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 novel 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, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous 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 framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

为了研究脊椎动物适应性辐射的起源和阶段，我们从 202 条加勒比海鲽的基因组中重建了作为多样化主要表型轴基础的适应性等位基因的时空历史。在一个巴哈马岛上，来自不同地理来源的古老变异在强烈的定向选择下被重新组合成新的组合，以适应新的鳞食性和软体动物的营养生态位。我们发现了适应性辐射的两个长期假设的证据：混合群起源和适应的时间阶段。结合群体基因组学、转录组学和全基因组关联作图，我们证明了圣萨尔瓦多岛上新型营养专家的这种微地方性适应性辐射，巴哈马经历的适应性基因渗入是邻近岛屿上的通才种群的两倍，并且适应性分化是分阶段发生的。首先，与摄食行为相关的基因存在调节性变异（prlh、cfap20和rmi1）被选择固定，然后在与颅面和肌肉发育相关的基因（itga5、ext1、cyp26b1和galr2）中保持调节变异，最后是成骨转录因子中唯​​一的从头非同义替代和癌基因 ( twist1 ) 最近被固定。我们的结果证明了在不同环境避难所中维持的古老等位基因如何组装成新的适应性组合，并为重建适应和物种形成的时空景观提供框架。