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

Research output: Contribution to journalArticle

Authors

  • Thomas H Hampton
  • Benjamin L King
  • Andrew Whitehead
  • Fernando Galvez
  • Robert H Gross
  • Nathan Keith
  • Emily Notch
  • Dawoon Jung
  • Stephen P Glaholt
  • Celia Y Chen
  • Bruce A Stanton

Colleges, School and Institutes

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.

Details

Original languageEnglish
Pages (from-to)3002-15
Number of pages14
JournalMolecular Biology and Evolution
Volume31
Issue number11
Early online date25 Aug 2014
Publication statusPublished - Nov 2014

Keywords

  • Adaptation, Physiological, Animals, Arsenic, Biological Evolution, Fish Proteins, Fresh Water, Fundulidae, Gene Expression Regulation, Gene Regulatory Networks, Gene-Environment Interaction, Genome, Gills, Male, Phenotype, Salinity, Salts, Seawater, Selection, Genetic