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Title: Genetic basis for evolved tolerance to dioxin-like pollutants in wild atlantic killifish: more than the aryl hydrocarbon receptor

Author
item NACCI, DIANE - Environmental Protection Agency (EPA)
item Proestou, Dina
item CHAMPLIN, DENISE - Environmental Protection Agency (EPA)
item MARTINSON, JOHN - Environmental Protection Agency (EPA)
item WAITS, ERIC - Environmental Protection Agency (EPA)

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/30/2016
Publication Date: 10/20/2016
Citation: Nacci, D., Proestou, D.A., Champlin, D., Martinson, J., Waits, E. 2016. Genetic basis for evolved tolerance to dioxin-like pollutants in wild atlantic killifish: more than the aryl hydrocarbon receptor. Molecular Ecology. 25(21):5467-5482.

Interpretive Summary: A classic breeding design and molecular genetic markers were used to characterize the genetic basis for contemporary evolution in a wild fish species with ‘sufficient genetic resources’- many genetically variable individuals- to adapt to PCB contamination in a US superfund site. In vertebrates, toxic responses to PCBs are largely controlled by a nuclear receptor. In this study, several genes, acting singly and in combination, were more strongly associated with this adaptation than the receptor itself. The rapid, independent and simultaneous development of evolved tolerance via similar but not identical genetic mechanisms in multiple populations of once common estuarine fish advance our understanding of genetic mechanisms that may buffer risks to the persistence of wild species in a rapidly changing environment.

Technical Abstract: Atlantic killifish (Fundulus heteroclitus) resident to some US urban and industrialized estuaries demonstrate recently evolved and extreme tolerance to toxic dioxin-like compounds (DLCs). Here we provide an unusually comprehensive accounting (69%) through Quantitative Trait Locus (QTL) analysis of the genetic basis for DLC tolerance in killifish resident to a PCB-contaminated Superfund site. Consistent with mechanistic knowledge of DLC toxicity in fish and other vertebrates, the aryl hydrocarbon receptor (ahr2) region accounts for 17% of trait variation; however, QTLs on an independent linkage group and their interactions have even greater explanatory power (44%). Some QTLs were also enriched in geographically disparate DLC-tolerant killifish populations, suggesting convergence in this independently evolving intra-specific trait. Results interpreted by leveraging Fundulus genomic resources and shared synteny among fish species suggest adaptation via inter-acting components of a complex stress response network, and provide new insight into genetic mechanisms of rapid evolution in the wild.