A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape
A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape
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DOI：
10.1073/pnas.2011811118
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发表时间：
2021-05
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影响因子：
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通讯作者：
E. Richards;J. A. McGirr;Jeremy R. Wang;M. S. St. John;J. Poelstra;Maria J. Solano;Delaney C. O’Connell;B. Turner;C. Martin
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作者：
E. Richards;J. A. McGirr;Jeremy R. Wang;M. S. St. John;J. Poelstra;Maria J. Solano;Delaney C. O’Connell;B. Turner;C. Martin
意义 大多数生物多样性是在新物种、适应性和生态位的快速爆发中进化而来的。然而，人们对这种适应性辐射的过程知之甚少。我们对整个加勒比地区的鳉鱼进行了大规模基因组测序，以了解为什么该群体的辐射仅限于巴哈马的一个岛屿。我们发现，流向这个岛屿的基因流增加了一倍，带来了古代适应性突变的新组合，这些突变是殖民食鳞和食蜗牛的新生态位所需的。适应分阶段进行：首先选择摄食行为，然后选择营养形态，最后通过基因编码变化进行细化。我们证明，年轻的局部辐射可以从跨越时间和空间传播的大量适应性遗传变异中产生。为了研究脊椎动物适应性辐射的起源和阶段，我们从 202 条加勒比海鳉鱼的基因组中重建了多样化主要表型轴下的适应性等位基因的空间和时间历史。在巴哈马的一个岛屿上，来自不连续地理来源的古代常备变异在强烈的定向选择下被重新组合成新的组合，以适应食鳞和软体动物的新营养位。我们找到了关于适应性辐射的两个长期存在的假设的证据：混合群起源和适应的时间阶段。通过结合群体基因组学、转录组学和全基因组关联图谱，我们证明了巴哈马圣萨尔瓦多岛上新型营养专家的这种微流行适应性辐射经历的适应性渐渗是邻近岛屿上普通群体的两倍，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（prlh、cfap20和rmi1）的常设调节变异通过选择被固定，然后与颅面和肌肉发育相关的基因（itga5、ext1、cyp26b1和galr2）的常设调节变异，最后是成骨转录因子和癌基因（twist1）中唯一的从头非同义取代，最近被固定。我们的结果证明了在不同环境保护区中维持的古代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。
Significance Most biodiversity evolved in rapid bursts of new species, adaptations, and ecological niches. However, this process of adaptive radiation is poorly understood. We used large-scale genomic sequencing across the entire Caribbean range of pupfishes to understand why radiation in this group is restricted to a single Bahamian island. We found that twofold higher gene flow to this island brought in new combinations of ancient adaptive mutations needed for colonizing novel ecological niches of scale-eating and snail-eating. Adaptation occurred in stages: first selection on feeding behavior, then selection for trophic morphology, and finally refinement through gene coding change. We demonstrate that young, localized radiations can emerge from a vast pool of adaptive genetic variation spread across time and space. 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.