A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape
Autors
Emilie J. Richardsa, Joseph A. McGirrc, Jeremy R. Wangd, Michelle E. St. Johna, Jelmer W. Poelstrae, Maria J. Solanof, Delaney C. O’Connellf, Bruce J. Turnerg and Christopher H. Martina
Department of Integrative Biology, University of California, Berkeley, CA 94720 Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720 Department of Environmental Toxicology, University of California, Davis, CA 95616 Department of Genetics, University of North Carolina, Chapel Hill, NC 27514 Molecular and Cellular Imaging Center, Ohio State University, Columbus, OH 43210 Department of Biology, University of North Carolina, Chapell Hill, NC 27514 Department of Biological Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24601 Edited by Peter R. Grant, Princeton University, Princeton, NJ, and approved March 15, 2021 (received for review June 11, 2020)
Aspect
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 andmolluscivory. 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 tha 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 facto and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmentalrefugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.
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