A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape

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.

Medienart:

E-Artikel

Erscheinungsjahr:

2021

Erschienen:

2021

Enthalten in:

Zur Gesamtaufnahme - volume:118

Enthalten in:

Proceedings of the National Academy of Sciences of the United States of America - 118(2021), 20 vom: 18. Mai

Sprache:

Englisch

Beteiligte Personen:

Richards, Emilie J [VerfasserIn]
McGirr, Joseph A [VerfasserIn]
Wang, Jeremy R [VerfasserIn]
St John, Michelle E [VerfasserIn]
Poelstra, Jelmer W [VerfasserIn]
Solano, Maria J [VerfasserIn]
O'Connell, Delaney C [VerfasserIn]
Turner, Bruce J [VerfasserIn]
Martin, Christopher H [VerfasserIn]

Links:

Volltext

Themen:

Adaptation
Adaptive radiation
Fish Proteins
Genomics
Hybridization
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Speciation

Anmerkungen:

Date Completed 06.12.2021

Date Revised 14.12.2021

published: Print

Citation Status MEDLINE

doi:

10.1073/pnas.2011811118

funding:

Förderinstitution / Projekttitel:

PPN (Katalog-ID):

NLM325418128