Journal
MOLECULAR BIOLOGY AND EVOLUTION
Volume 31, Issue 11, Pages 3002-3015Publisher
OXFORD UNIV PRESS
DOI: 10.1093/molbev/msu241
Keywords
phenotypic plasticity; canalization; evolution; gene regulatory networks; natural populations
Funding
- BioProject [PRJNA201069]
- National Institute of Environmental Health Sciences (NIEHS) Superfund Basic Research Program [P42 ES007373]
- NIEHS [R01 ES019324]
- Department of Defense-Strategic Environmental Research and Development Program [ER1503]
- National Institute of Health (NIH) [RO1 HL074175]
- NIH [P20 GM103423, P20 GM104318]
- National Science Foundation (NSF) [DEB-1120512]
- NSF [DBI-0445967, EF-0723771]
- METACyt Initiative of IU, through Lilly Endowment, Inc.
- Direct For Biological Sciences
- Division Of Environmental Biology [1265282] Funding Source: National Science Foundation
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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.
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