|REID, NOAH - University Of California|
|CLARK, BRYAN - Environmental Protection Agency (EPA)|
|WARREN, WESLEY - Washington University|
|COLBOURNE, JOHN - University Of Birmingham|
|SHAW, JOSEPH - Indiana University|
|KARCHNER, SIBEL - Woods Hole Oceanographic Institute (WHOI)|
|HAHN, MARK - Woods Hole Oceanographic Institute (WHOI)|
|NACCI, DIANE - Environmental Protection Agency (EPA)|
|OLEKSIAK, MARJORIE - University Of Miami|
|CRAWFORD, DOUGLAS - University Of Miami|
|WHITEHEAD, ANDREW - University Of California|
Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/31/2016
Publication Date: 12/9/2016
Citation: Reid, N.M., Proestou, D.A., Clark, B.W., Warren, W.C., Colbourne, J.K., Shaw, J.R., Karchner, S.I., Hahn, M.E., Nacci, D., Oleksiak, M.F., Crawford, D.J., Whitehead, A. 2016. The genomic landscape of rapid, repeated evolutionary rescue from toxic pollution in wild fish. Science. 354(6317):1305-1308.
Interpretive Summary: The rate and magnitude of evolutionary change depends on the existence of genetic variation, population size, and intensity of selection. Population genomic and transcriptomic analyses were used to reveal how multiple populations of an abundant and widely distributed estuarine fish have rapidly adapted to dramatic, human-induced environmental change. Few candidate regions underlying tolerance to complex mixtures of polycyclic and halogenated aromatic hydrocarbons were shared among the four tolerant fish populations examined; however, those that were shared were very highly ranked, suggesting the most important targets of selection have evolved in parallel across polluted sites. Common candidate regions include the aryl hydrocarbon receptor (AHR) locus, a region containing the aryl hydrocarbon receptor interacting protein (AIP) locus, and a region containing the cytochrome p450 1A (CYP1A) locus; all components of the AHR detoxification pathway. Despite the overlap of highly ranked candidate regions under selection among tolerant populations, multiple molecular variants associated with tolerance exist at each of these loci. In addition, genes beyond the AHR pathway were found to be important components of the tolerant phenotype in some, but not all populations. Because the AHR pathway has diverse functions and interacts with multiple signaling pathways, evolution of genes from other pathways that interact with the AHR may reflect compensatory adaptation.
Technical Abstract: Here we describe evolutionary rescue from intense pollution via multiple modes of selection in killifish populations from 4 urban estuaries of the US eastern seaboard. Comparative transcriptomics and analysis of 384 whole genome sequences show that the functioning of a receptor-based signaling pathway, and its regulating genes, are the repeated targets of natural selection, yet different molecular variants are sometimes recruited in different populations. The pathway under strong selection normally exhibits crosstalk with other signaling pathways within which we also detect selection, indicating compensatory adaptations. Selection also targets toxicity-mediating genes outside of this pathway, indicating that the tolerance phenotype is complex. High nucleotide diversity and extensive pre-existing genetic variation have been crucial substrates for selective sweeps to propel evolutionary rescue.