Warren
Wesley C.
Warren
Wesley C.
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ArticleThe landscape of extreme genomic variation in the highly adaptable Atlantic killifish(Oxford University Press, 2017-03-01) Reid, Noah M. ; Jackson, Craig E. ; Gilbert, Don ; Minx, Patrick ; Montague, Michael J. ; Hampton, Thomas H. ; Helfrich, Lily W. ; King, Benjamin L. ; Nacci, Diane E. ; Aluru, Neelakanteswar ; Karchner, Sibel I. ; Colbourne, John K. ; Hahn, Mark E. ; Shaw, Joseph R. ; Oleksiak, Marjorie F. ; Crawford, Douglas L. ; Warren, Wesley C. ; Whitehead, AndrewUnderstanding and predicting the fate of populations in changing environments require knowledge about the mechanisms that support phenotypic plasticity and the adaptive value and evolutionary fate of genetic variation within populations. Atlantic killifish (Fundulus heteroclitus) exhibit extensive phenotypic plasticity that supports large population sizes in highly fluctuating estuarine environments. Populations have also evolved diverse local adaptations. To yield insights into the genomic variation that supports their adaptability, we sequenced a reference genome and 48 additional whole genomes from a wild population. Evolution of genes associated with cell cycle regulation and apoptosis is accelerated along the killifish lineage, which is likely tied to adaptations for life in highly variable estuarine environments. Genome-wide standing genetic variation, including nucleotide diversity and copy number variation, is extremely high. The highest diversity genes are those associated with immune function and olfaction, whereas genes under greatest evolutionary constraint are those associated with neurological, developmental, and cytoskeletal functions. Reduced genetic variation is detected for tight junction proteins, which in killifish regulate paracellular permeability that supports their extreme physiological flexibility. Low-diversity genes engage in more regulatory interactions than high-diversity genes, consistent with the influence of pleiotropic constraint on molecular evolution. High genetic variation is crucial for continued persistence of species given the pace of contemporary environmental change. Killifish populations harbor among the highest levels of nucleotide diversity yet reported for a vertebrate species, and thus may serve as a useful model system for studying evolutionary potential in variable and changing environments.
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PreprintThe genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish( 2016-10) Reid, Noah M. ; Proestou, Dina A. ; Clark, Bryan W. ; Warren, Wesley C. ; Colbourne, John K. ; Shaw, Joseph R. ; Karchner, Sibel I. ; Hahn, Mark E. ; Nacci, Diane E. ; Oleksiak, Marjorie F. ; Crawford, Douglas L. ; Whitehead, AndrewAtlantic killifish populations have rapidly adapted to normally lethal levels of pollution in four urban estuaries. Through analysis of 384 whole killifish genome sequences and comparative transcriptomics in four pairs of sensitive and tolerant populations, we identify the aryl hydrocarbon receptor-based signaling pathway as a shared target of selection. This suggests evolutionary constraint on adaptive solutions to complex toxicant mixtures at each site. However, distinct molecular variants apparently contribute to adaptive pathway modification among tolerant populations. Selection also targets other toxicity-mediating genes, and genes of connected signaling pathways, indicating complex tolerance phenotypes and potentially compensatory adaptations. Molecular changes are consistent with selection on standing genetic variation. In killifish high nucleotide diversity has likely been a crucial substrate for selective sweeps to propel rapid adaptation.