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Mol Biol Evol. 2014 Nov;31(11):3002-15. doi: 10.1093/molbev/msu241. Epub 2014 Aug 25.

Natural selection canalizes expression variation of environmentally induced plasticity-enabling genes.

Author information

1
The School of Public and Environmental Affairs, Indiana University, Bloomington The Center for Genomics and Bioinformatics, Indiana University, Bloomington The Mount Desert Island Biological Laboratory, Salisbury Cove, ME Environmental Genomics Group, School of Biosciences, University of Birmingham, Birmingham, United Kingdom joeshaw@indiana.edu.
2
Environmental Genomics Group, School of Biosciences, University of Birmingham, Birmingham, United Kingdom Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH.
3
The Mount Desert Island Biological Laboratory, Salisbury Cove, ME.
4
Department of Environmental Toxicology, University of California, Davis.
5
Department of Biological Sciences, Louisiana State University, Baton Rouge.
6
Department of Biological Sciences, Dartmouth College, Hanover, NH.
7
The School of Public and Environmental Affairs, Indiana University, Bloomington.
8
The Mount Desert Island Biological Laboratory, Salisbury Cove, ME Department of Microbiology and Immunology, Geisel School of Medicine at Dartmouth, Hanover, NH.
9
The Center for Genomics and Bioinformatics, Indiana University, Bloomington The Mount Desert Island Biological Laboratory, Salisbury Cove, ME Environmental Genomics Group, School of Biosciences, University of Birmingham, Birmingham, United Kingdom.

Abstract

Many organisms survive fluctuating and extreme environmental conditions by manifesting multiple distinct phenotypes during adulthood by means of developmental processes that enable phenotypic plasticity. We report on the discovery of putative plasticity-enabling genes that are involved in transforming the gill of the euryhaline teleost fish, Fundulus heteroclitus, from its freshwater to its seawater gill-type, a process that alters both morphology and function. Gene expression that normally enables osmotic plasticity is inhibited by arsenic. Gene sets defined by antagonistic interactions between arsenic and salinity show reduced transcriptional variation among individual fish, suggesting unusually accurate and precise regulatory control of these genes, consistent with the hypothesis that they participate in a canalized developmental response. We observe that natural selection acts to preserve canalized gene expression in populations of killifish that are most tolerant to abrupt salinity change and that these populations show the least variability in their transcription of genes enabling plasticity of the gill. We found that genes participating in this highly canalized and conserved plasticity-enabling response had significantly fewer and less complex associations with transcriptional regulators than genes that respond only to arsenic or salinity. Collectively these findings, which are drawn from the relationships between environmental challenge, plasticity, and canalization among populations, suggest that the selective processes that facilitate phenotypic plasticity do so by targeting the regulatory networks that gives rise to the response. These findings also provide a generalized, conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits.

KEYWORDS:

canalization; evolution; gene regulatory networks; natural populations; phenotypic plasticity

PMID:
25158801
PMCID:
PMC4209136
DOI:
10.1093/molbev/msu241
[Indexed for MEDLINE]
Free PMC Article

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