Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 118, Issue 20, Pages -Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2011811118
Keywords
adaptive radiation; speciation; genomics; adaptation; hybridization
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Funding
- NIH [S10 OD018174, 5R01DE027052-02]
- NSF Division of Environmental Biology (DEB) CAREER grant [1749764]
- Museum of Vertebrate Zoology
- University of North Carolina at Chapel Hill
- University of California, Berkeley
- Division Of Environmental Biology
- Direct For Biological Sciences [1749764] Funding Source: National Science Foundation
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This study investigated the evolutionary origins and stages of vertebrate adaptive radiation using the genomes of 202 Caribbean pupfishes. They found evidence supporting hybrid swarm origins and temporal stages of adaptation in an adaptive radiation event on San Salvador Island, Bahamas. The research demonstrates how ancient alleles from different environmental refugia can be reassembled into new adaptive combinations, providing insights into the spatiotemporal landscape of adaptation and speciation.
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.
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