Organisms adapted to physiochemical stressors provide ideal systems to study evolutionary mechanisms that drive adaptation and speciation. This review study focuses on livebearing fishes of the
- NSF-PAR ID:
- 10215422
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 117
- Issue:
- 28
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 16424 to 16430
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Poecilia mexicana species complex (Poeciliidae), members of which have repeatedly colonized hydrogen sulphide (H2S)‐rich springs. H2S is a potent respiratory toxicant that creates extreme environmental conditions in aquatic ecosystems. There is also a rich history of research on H2S in toxicology and biomedicine, which has facilitated the generation of a priori hypotheses about the proximate mechanisms of adaptation. Testing these hypotheses through the application of high‐throughput genomic and transcriptomic analyses has led to the identification of the physiological underpinnings mediating adaptation to H2S‐rich environments. In addition, systematic natural history studies have provided a nuanced understanding of how the presence of a physiochemical stressor interacts with other sources of selection to drive evolutionary change in a variety of organismal traits, including physiology, morphology, behaviour and life history. Adaptation to extreme environments inP. mexicana also coincides with ecological speciation, and evolutionarily independent lineages span almost the full range of the speciation continuum from panmixia to complete reproductive isolation. Multiple mechanisms of reproductive isolation are involved in reducing gene flow between adjacent populations that are adapted to contrasting environmental conditions. Comparative studies among evolutionarily independent lineages within theP. mexicana species complex and, more recently, other members of the family Poeciliidae that have colonized H2S‐rich environments will provide insights into the factors facilitating or impeding convergent evolution, providing tangible links between micro‐evolutionary processes and macro‐evolutionary patterns. -
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Abstract microRNAs (miRNAs) are post‐transcriptional regulators of gene expression and can play an important role in modulating organismal development and physiology in response to environmental stress. However, the role of miRNAs in mediating adaptation to diverse environments in natural study systems remains largely unexplored. Here, we characterized miRNAs and their expression in
Poecilia mexicana , a species of small fish that inhabits both normal streams and extreme environments in the form of springs rich in toxic hydrogen sulphide (H2S). We found thatP. mexicana has a similar number of miRNA genes as other teleosts. In addition, we identified a large population of mature miRNAs that were differentially expressed between locally adapted populations in contrasting habitats, indicating that miRNAs may contribute toP. mexicana adaptation to sulphidic environments. In silico identification of differentially expressed miRNA‐mRNA pairs revealed, in the sulphidic environment, the downregulation of miRNAs predicted to target mRNAs involved in sulphide detoxification and cellular homeostasis, which are pathways essential for life in H2S‐rich springs. In addition, we found that predicted targets of upregulated miRNAs act in the mitochondria (16.6% of predicted annotated targets), which is the main site of H2S toxicity and detoxification, possibly modulating mitochondrial function. Together, the differential regulation of miRNAs between these natural populations suggests that miRNAs may be involved in H2S adaptation by promoting functions needed for survival and reducing functions affected by H2S. This study lays the groundwork for further research to directly demonstrate the role of miRNAs in adaptation to H2S. Overall, this study provides a critical stepping‐stone towards a comprehensive understanding of the regulatory mechanisms underlying the adaptive variation in gene expression in a natural system. -
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Abstract 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. -
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Abstract Hydrogen sulfide is a toxic gas that disrupts numerous biological processes, including energy production in the mitochondria, yet fish in the
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Environmental factors can promote phenotypic variation through alterations in the epigenome and facilitate adaptation of an organism to the environment. Although hydrogen sulfide is toxic to most organisms, the fish Poecilia mexicana has adapted to survive in environments with high levels that exceed toxicity thresholds by orders of magnitude. Epigenetic changes in response to this environmental stressor were examined by assessing DNA methylation alterations in red blood cells, which are nucleated in fish. Males and females were sampled from sulfidic and nonsulfidic natural environments; individuals were also propagated for two generations in a nonsulfidic laboratory environment. We compared epimutations between the sexes as well as field and laboratory populations. For both the wild-caught (F0) and the laboratory-reared (F2) fish, comparing the sulfidic and nonsulfidic populations revealed evidence for significant differential DNA methylation regions (DMRs). More importantly, there was over 80% overlap in DMRs across generations, suggesting that the DMRs have stable generational inheritance in the absence of the sulfidic environment. This is an example of epigenetic generational stability after the removal of an environmental stressor. The DMR-associated genes were related to sulfur toxicity and metabolic processes. These findings suggest that adaptation of P. mexicana to sulfidic environments in southern Mexico may, in part, be promoted through epigenetic DNA methylation alterations that become stable and are inherited by subsequent generations independent of the environment.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2004223117
