Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae)

Courtney N. Passow, Anthony P. Brown, Lenin Arias-Rodriguez, Muh Ching Yee, Alexandra Sockell, Manfred Schartl, Wesley C. Warren, Carlos Bustamante, Joanna L. Kelley, Michael Tobler

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Variation in gene expression can provide insights into organismal responses to environmental stress and physiological mechanisms mediating adaptation to habitats with contrasting environmental conditions. We performed an RNA-sequencing experiment to quantify gene expression patterns in fish adapted to habitats with different combinations of environmental stressors, including the presence of toxic hydrogen sulphide (H2S) and the absence of light in caves. We specifically asked how gene expression varies among populations living in different habitats, whether population differences were consistent among organs, and whether there is evidence for shared expression responses in populations exposed to the same stressors. We analysed organ-specific transcriptome-wide data from four ecotypes of Poecilia mexicana (nonsulphidic surface, sulphidic surface, nonsulphidic cave and sulphidic cave). The majority of variation in gene expression was correlated with organ type, and the presence of specific environmental stressors elicited unique expression differences among organs. Shared patterns of gene expression between populations exposed to the same environmental stressors increased with levels of organismal organization (from transcript to gene to physiological pathway). In addition, shared patterns of gene expression were more common between populations from sulphidic than populations from cave habitats, potentially indicating that physiochemical stressors with clear biochemical consequences can constrain the diversity of adaptive solutions that mitigate their adverse effects. Overall, our analyses provided insights into transcriptional variation in a unique system, in which adaptation to H2S and darkness coincide. Functional annotations of differentially expressed genes provide a springboard for investigating physiological mechanisms putatively underlying adaptation to extreme environments.

Original languageEnglish (US)
Pages (from-to)4211-4225
Number of pages15
JournalMolecular ecology
Volume26
Issue number16
DOIs
StatePublished - Aug 2017

Bibliographical note

Funding Information:
We would like to thank N. Franssen for assistance collecting field samples and the Centro de Investigaci?n e Innovaci?n para la Ense?anza y Aprendizaje (CIIEA) for providing logistical support. We also thank the Oklahoma State University High Performance Computing Center (OSUHPCC) for providing access, support and resources, especially D. Brunson and J. Schafer for all their guidance. 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 and a Vern Parish Award from the American Livebearer Association to CNP, as well as grants from the National Science Foundation (IOS-1121832, IOS-1463720, IOS-1557860 and IOS-1557795) and the U.S. Army Research Office (W911NF-15-1-0175) to MT and JLK. Genome reference work was supported by a grant to WCW (NIH: 2R24OD011198-04A1).

Publisher Copyright:
© 2017 John Wiley & Sons Ltd

Keywords

  • caves
  • extreme environments
  • hydrogen sulphide
  • local adaptation
  • poeciliidae
  • transcriptomes

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