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

5 years ago

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

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

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 and 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 sulfide (H2S)-rich springs and adjacent nontoxic habitats, and assessed genome-wide 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 sulfidic and nonsulfidic 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, sulfur 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. This article is protected by copyright. All rights reserved.

Publisher URL: http://onlinelibrary.wiley.com/resolve/doi

DOI: 10.1111/mec.14360