The roles of plasticity and evolutionary change in shaping gene expression variation in natural populations of extremophile fish

Courtney N. Passow, Chathurika Henpita, Jennifer H. Shaw, Corey R. Quackenbush, Wesley C. Warren, Manfred Schartl, Lenin Arias-Rodriguez, Joanna L. Kelley, Michael Tobler

Research output: Contribution to journalArticlepeer-review

18 Scopus citations


The notorious plasticity of gene expression responses and the complexity of environmental gradients complicate the identification of adaptive differences in gene regulation among populations. We combined transcriptome analyses in nature with common-garden and exposure experiments to establish cause–effect relationships between the presence of a physiochemical stressor and expression differences, as well as to test how evolutionary change and plasticity interact to shape gene expression variation in natural systems. We studied two evolutionarily independent population pairs of an extremophile fish (Poecilia mexicana) living in toxic, hydrogen sulphide (H2S)-rich springs and adjacent nontoxic habitats and assessed genomewide expression patterns of wild-caught and common-garden-raised individuals exposed to different concentrations of H2S. We found that 7.7% of genes that were differentially expressed between sulphidic and nonsulphidic ecotypes remained differentially expressed in the laboratory, indicating that sources of selection other than H2S—or plastic responses to other environmental factors—contribute substantially to gene expression patterns observed in the wild. Concordantly differentially expressed genes in the wild and the laboratory were primarily associated with H2S detoxification, sulphur processing and metabolic physiology. While shared, ancestral plasticity played a minor role in shaping gene expression variation observed in nature, we documented evidence for evolved population differences in the constitutive expression as well as the H2S inducibility of candidate genes. Mechanisms underlying gene expression variation also varied substantially across the two ecotype pairs. These results provide a springboard for studying evolutionary modifications of gene regulatory mechanisms that underlie expression variation in locally adapted populations.

Original languageEnglish (US)
Pages (from-to)6384-6399
Number of pages16
JournalMolecular ecology
Issue number22
StatePublished - Nov 2017

Bibliographical note

Funding Information:
We thank Z. W. Culumber, T. Doumas and R. Greenway for assistance in collecting field samples, as well as A. Brown and M.-C. Yee for aiding in library preparation and logistics. We also thank Centro de Investigación e Innovación para la Enseñanza y Aprendizaje (CIIEA) for logistical support during fieldwork. Dana Brunson and Jesse Schafer of the Oklahoma State University High Performance Computing Center (OSUHPCC) provided access, support and resources. Permits were provided by the Mexican government (DGOPA.00093.120110.-0018). Research was supported by a Fellowship of Graduate Student Travel from the Society of Integrative and Comparative Biology to CNP, grants from the National Science Foundation (IOS-1463720 and IOS-1557860 to MT; IOS-1557795 to JLK), the U.S. Army Research Office (W911NF-15-1-0175 to MT and JLK) and the Defense University Research Instrumentation Program of the U.S. office Naval Research (W911NF-16-1-0225 to MT) as well as a Ralph E. Powe Junior Faculty Enhancement Award from Oak Ridge Associated Universities to MT. Genome reference work was supported by an NIH grant to WCW (2R24OD011198-04A1).

Funding Information:
NIH Clinical Center, Grant/Award Number: 2R24OD011198-04A1; National Science Foundation, Grant/Award Number: IOS-1463720, IOS-1557860, IOS-1557795; U.S. Army Research Office, Grant/Award Number: W911NF-15-1-0175

Publisher Copyright:
© 2017 John Wiley & Sons Ltd


  • Poecilia mexicana (Poeciliidae)
  • adaptation
  • gene regulation
  • hydrogen sulphide
  • plasticity
  • transcriptome


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