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

Abstract

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 terrestrialmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [4];  [5]
  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, Superfund Research Program Boston University Boston MA USA
  5. Atlantic Ecology Division National Health and Environmental Effects Research Laboratory Office of Research and Development US Environmental Protection Agency Narragansett RI USA
Publication Date:
Research Org.:
Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1353288
Alternate Identifier(s):
OSTI ID: 1353289; OSTI ID: 1625870
Grant/Contract Number:  
SC0014664
Resource Type:
Published Article
Journal Name:
Evolutionary Applications
Additional Journal Information:
Journal Name: Evolutionary Applications Journal Volume: 10 Journal Issue: 8; Journal ID: ISSN 1752-4571
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
Evolutionary Biology; adaptation; contemporary evolution; ecological genetics; ecotoxicology; genomics/proteomics; molecular evolution; natural selection and contemporary evolution; population genetics—empirical

Citation Formats

Whitehead, Andrew, Clark, Bryan W., Reid, Noah M., Hahn, Mark E., and Nacci, Diane. When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus ) populations. United Kingdom: N. p., 2017. Web. doi:10.1111/eva.12470.
Whitehead, Andrew, Clark, Bryan W., Reid, Noah M., Hahn, Mark E., & Nacci, Diane. When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus ) populations. United Kingdom. https://doi.org/10.1111/eva.12470
Whitehead, Andrew, Clark, Bryan W., Reid, Noah M., Hahn, Mark E., and Nacci, Diane. Wed . "When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus ) populations". United Kingdom. https://doi.org/10.1111/eva.12470.
@article{osti_1353288,
title = {When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus ) populations},
author = {Whitehead, Andrew and Clark, Bryan W. and Reid, Noah M. and Hahn, Mark E. and Nacci, Diane},
abstractNote = {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.},
doi = {10.1111/eva.12470},
journal = {Evolutionary Applications},
number = 8,
volume = 10,
place = {United Kingdom},
year = {Wed Apr 26 00:00:00 EDT 2017},
month = {Wed Apr 26 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/eva.12470

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Cited by: 83 works
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Figures / Tables:

Figure 1 Figure 1: Population variation in killifish larval survival when challenged with increasing exposure concentrations of PCB126. Modeled responses from repeated laboratory tests show that populations from polluted sites (solid curves) exhibit tolerance to pollutants at concentrations hundreds to thousands of times normally lethal levels (sensitive populations, dashed curves). Populations aremore » indicated by colors as shown in the map, which shows locations of tolerant populations (solid circles: New Bedford Harbor [NBH], Bridgeport [BP], Newark [NWK], and Elizabeth River [ER] from north to south) and sensitive reference populations (open circles: Block Island [BI], Flax Pond [FP], Sandy Hook [SH], and Kings Creek [KC], from north to south). PCB, polychlorinated biphenyl« less

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Heritable Adaptation and Fitness Costs in Killifish (Fundulus Heteroclitus) Inhabiting a Polluted Estuary
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GENETIC BASIS OF A BETWEEN-ENVIRONMENT TRADE-OFF INVOLVING RESISTANCE TO CADMIUM IN DROSOPHILA MELANOGASTER
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Fitness cost of Resistance to Cadmium in the Least Killifish (Heterandria Formosa)
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Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs)
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Estrogen responses in killifish (Fundulus heteroclitus) from polluted and unpolluted environments are site- and gene-specific
journal, August 2010


AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus)
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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.