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      When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus) populations

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          Abstract

          For most species, evolutionary adaptation is not expected to be sufficiently rapid to buffer the effects of human‐mediated environmental changes, including environmental pollution. Here we review how key features of populations, the characteristics of environmental pollution, and the genetic architecture underlying adaptive traits, may interact to shape the likelihood of evolutionary rescue from pollution. Large populations of Atlantic killifish (Fundulus heteroclitus) persist in some of the most contaminated estuaries of the United States, and killifish studies have provided some of the first insights into the types of genomic changes that enable rapid evolutionary rescue from complexly degraded environments. We describe how selection by industrial pollutants and other stressors has acted on multiple populations of killifish and posit that extreme nucleotide diversity uniquely positions this species for successful evolutionary adaptation. Mechanistic studies have identified some of the genetic underpinnings of adaptation to a well‐studied class of toxic pollutants; however, multiple genetic regions under selection in wild populations seem to reflect more complex responses to diverse native stressors and/or compensatory responses to primary adaptation. The discovery of these pollution‐adapted killifish populations suggests that the evolutionary influence of anthropogenic stressors as selective agents occurs widely. Yet adaptation to chemical pollution in terrestrial and aquatic vertebrate wildlife may rarely be a successful “solution to pollution” because potentially adaptive phenotypes may be complex and incur fitness costs, and therefore be unlikely to evolve quickly enough, especially in species with small population sizes.

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          Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments

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            Aryl hydrocarbon receptor control of a disease tolerance defence pathway.

            Disease tolerance is the ability of the host to reduce the effect of infection on host fitness. Analysis of disease tolerance pathways could provide new approaches for treating infections and other inflammatory diseases. Typically, an initial exposure to bacterial lipopolysaccharide (LPS) induces a state of refractoriness to further LPS challenge (endotoxin tolerance). We found that a first exposure of mice to LPS activated the ligand-operated transcription factor aryl hydrocarbon receptor (AhR) and the hepatic enzyme tryptophan 2,3-dioxygenase, which provided an activating ligand to the former, to downregulate early inflammatory gene expression. However, on LPS rechallenge, AhR engaged in long-term regulation of systemic inflammation only in the presence of indoleamine 2,3-dioxygenase 1 (IDO1). AhR-complex-associated Src kinase activity promoted IDO1 phosphorylation and signalling ability. The resulting endotoxin-tolerant state was found to protect mice against immunopathology in Gram-negative and Gram-positive infections, pointing to a role for AhR in contributing to host fitness.
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              Maturation trends indicative of rapid evolution preceded the collapse of northern cod.

              Northern cod, comprising populations of Atlantic cod (Gadus morhua) off southern Labrador and eastern Newfoundland, supported major fisheries for hundreds of years. But in the late 1980s and early 1990s, northern cod underwent one of the worst collapses in the history of fisheries. The Canadian government closed the directed fishing for northern cod in July 1992, but even after a decade-long offshore moratorium, population sizes remain historically low. Here we show that, up until the moratorium, the life history of northern cod continually shifted towards maturation at earlier ages and smaller sizes. Because confounding effects of mortality changes and growth-mediated phenotypic plasticity are accounted for in our analyses, this finding strongly suggests fisheries-induced evolution of maturation patterns in the direction predicted by theory. We propose that fisheries managers could use the method described here as a tool to provide warning signals about changes in life history before more overt evidence of population decline becomes manifest.
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                Author and article information

                Contributors
                awhitehead@ucdavis.edu
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                26 April 2017
                September 2017
                : 10
                : 8 , Evolutionary Toxicology ( doiID: 10.1111/eva.2017.10.issue-8 )
                : 762-783
                Affiliations
                [ 1 ] Department of Environmental Toxicology University of California Davis Davis CA USA
                [ 2 ] Atlantic Ecology Division National Health and Environmental Effects Research Laboratory Office of Research and Development Oak Ridge Institute for Science and Education US Environmental Protection Agency Narragansett RI USA
                [ 3 ] Department of Molecular and Cell Biology University of Connecticut Storrs CT USA
                [ 4 ] Department of Biology Woods Hole Oceanographic Institution Woods Hole MA USA
                [ 5 ] Superfund Research Program Boston University Boston MA USA
                [ 6 ] Atlantic Ecology Division National Health and Environmental Effects Research Laboratory Office of Research and Development US Environmental Protection Agency Narragansett RI USA
                Author notes
                [*] [* ] Correspondence

                Andrew Whitehead, Department of Environmental Toxicology, University of California Davis, Davis, CA, USA.

                Email: awhitehead@ 123456ucdavis.edu

                Author information
                http://orcid.org/0000-0002-5457-6449
                http://orcid.org/0000-0003-4358-2082
                Article
                EVA12470
                10.1111/eva.12470
                5680427
                29151869
                20075df1-9bff-41ad-a72f-83ecc0e02161
                © 2017 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 November 2016
                : 10 February 2017
                Page count
                Figures: 5, Tables: 0, Pages: 22, Words: 20960
                Funding
                Funded by: National Science Foundation
                Award ID: DEB‐1265282
                Award ID: OCE‐1314567
                Award ID: DEB‐1120263
                Funded by: National Institutes of Environmental Health Sciences
                Award ID: R01ES021934‐01
                Award ID: P42ES007381
                Funded by: Postdoctoral Research Program at the US Environmental Protection (US EPA)
                Funded by: Office of Research and Development
                Funded by: Oak Ridge Institute for Science and Education (ORISE)
                Award ID: DW92429801
                Funded by: US Department of Energy
                Categories
                Review and Syntheses
                Reviews and Syntheses
                Custom metadata
                2.0
                eva12470
                September 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.2.4.1 mode:remove_FC converted:10.11.2017

                Evolutionary Biology
                adaptation,contemporary evolution,ecological genetics,ecotoxicology,genomics/proteomics,molecular evolution,natural selection and contemporary evolution,population genetics—empirical

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