Department of Integrative Biology, University of California, Berkeley, CA 94720.
Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720.
Proc Natl Acad Sci U S A. 2021 May 18;118(20). doi: 10.1073/pnas.2011811118.
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 (, , and ) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (, , , and ) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene () 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 种加勒比短鲷的基因组中，重建了主要多样化表型轴背后的适应性等位基因的时空历史。在巴哈马的一个小岛上，来自不同地理来源的古老的固定变异，在适应新的摄食鳞片和食贝类的营养生态位的强烈定向选择下，被重新组合成新的组合。我们找到了支持适应性辐射的两个长期假设的证据：杂种群起源和适应的时间阶段。我们利用群体基因组学、转录组学和全基因组关联映射的组合，证明了这种在巴哈马圣萨尔瓦多岛上的新型营养专性辐射的微地方性适应性辐射，经历了比邻近岛屿的一般种群更多的适应性基因渗入，并且适应性分歧是分阶段发生的。首先，与摄食行为相关的基因（、、和）中的固定调控变异被选择固定，然后与颅面和肌肉发育相关的基因（、、、和）中的固定调控变异，以及最后，在一个成骨转录因子和癌基因（）中唯一的新非同义替换最近也被固定。我们的研究结果表明，如何将不同环境避难所中维持的古老等位基因组合成新的适应性组合，并为重建适应和物种形成的时空景观提供了一个框架。
