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Abstract Investigating closely related species that rapidly evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying variation in complex traits. This can also lead to the discovery of novel candidate genes influencing natural and clinical variation in human craniofacial phenotypes. We combined whole-genome resequencing of 258 individuals with 50 transcriptomes to identify candidate cis-acting genetic variation underlying rapidly evolving craniofacial phenotypes within an adaptive radiation of Cyprinodon pupfishes. This radiation consists of a dietary generalist species and two derived trophic niche specialists—a molluscivore and a scale-eating species. Despite extensive morphological divergence, these species only diverged 10 kya and produce fertile hybrids in the laboratory. Out of 9.3 million genome-wide SNPs and 80,012 structural variants, we found very few alleles fixed between species—only 157 SNPs and 87 deletions. Comparing gene expression across 38 purebred F1 offspring sampled at three early developmental stages, we identified 17 fixed variants within 10 kb of 12 genes that were highly differentially expressed between species. By measuring allele-specific expression in F1 hybrids from multiple crosses, we found that the majority of expression divergence between species was explained by trans-regulatory mechanisms. We also found strong evidence for two cis-regulatory alleles affecting expression divergence of two genes with putative effects on skeletal development (dync2li1 and pycr3). These results suggest that SNPs and structural variants contribute to the evolution of novel traits and highlight the utility of the San Salvador Island pupfish system as an evolutionary model for craniofacial development. 

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, andrmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5,ext1,cyp26b1, andgalr2) 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. 

Abstract Genomic methods are becoming increasingly valuable and established in ecological research, particularly in nonmodel species. Supporting their progress and adoption requires investment in resources that promote (i) reproducibility of genomic analyses, (ii) accessibility of learning tools and (iii) keeping pace with rapidly developing methods and principles.We introduce marineomics.io, an open‐source, living document to disseminate tutorials, reproducibility tools and best principles for ecological genomic research in marine and nonmodel systems.The website's existing content spans population and functional genomics, including current recommendations for whole‐genome sequencing, RAD‐seq, Pool‐seq and RNA‐seq. With the goal to facilitate the development of new, similar resources, we describe our process for aggregating and synthesizing methodological principles from the ecological genomics community to inform website content. We also detail steps for authorship and submission of new website content, as well as protocols for providing feedback and topic requests from the community.These web resources were constructed with guidance for doing rigorous, reproducible science. Collaboration and contributions to the website are encouraged from scientists of all skill sets and levels of expertise.