skip to main content


Title: microRNA expression variation as a potential molecular mechanism contributing to adaptation to hydrogen sulphide
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 inPoecilia 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. mexicanahas 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. mexicanaadaptation 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.

 
more » « less
Award ID(s):
1931650 1931657
NSF-PAR ID:
10363535
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Journal of Evolutionary Biology
Volume:
34
Issue:
6
ISSN:
1010-061X
Format(s):
Medium: X Size: p. 977-988
Size(s):
["p. 977-988"]
Sponsoring Org:
National Science Foundation
More Like this
  1. 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.

     
    more » « less
  2. Abstract

    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 thePoecilia mexicanaspecies 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. mexicanaalso 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. mexicanaspecies 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.

     
    more » « less
  3. Abstract

    The role of gene expression in adaptation to differing thermal environments has been assayed extensively. Yet, in most natural systems, analyses of gene expression reveal only one level of the complexity of regulatory machineries. MicroRNAs (miRNAs) are small noncoding RNAs which are key components of many gene regulatory networks, and they play important roles in a variety of cellular pathways by modulating post‐transcriptional quantities of mRNA available for protein synthesis. The characterization of miRNA loci and their regulatory dynamics in nonmodel systems are still largely understudied. In this study, we examine the role of miRNAs in response to high thermal stress in the intertidal copepodTigriopus californicus.Allopatric populations of this species show varying levels of local adaptation with respect to thermal regimes, and previous studies showed divergence in gene expression between populations from very different thermal environments. We examined the transcriptional response to temperature stress in two populations separated by only 8 km by utilizing RNA‐seq to quantify both mRNA and miRNA levels. Using the currently available genome sequence, we first describe the repertoire of miRNAs inT. californicusand assess the degree to which transcriptional response to temperature stress is governed by miRNA activity. The two populations showed large differences in the number of genes involved, the magnitude of change in commonly used genes and in the number of miRNAs involved in transcriptional modulation during stress. Our results suggest that an increased level of regulatory network complexity may underlie improved survivorship under thermal stress in one of the populations.

     
    more » « less
  4. null (Ed.)
    Extreme environments test the limits of life; yet, some organisms thrive in harsh conditions. Extremophile lineages inspire questions about how organisms can tolerate physiochemical stressors and whether the repeated colonization of extreme environments is facilitated by predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying convergent evolution of tolerance to hydrogen sulfide (H 2 S)—a toxicant that impairs mitochondrial function—across evolutionarily independent lineages of a fish ( Poecilia mexicana , Poeciliidae) from H 2 S-rich springs. Using comparative biochemical and physiological analyses, we found that mitochondrial function is maintained in the presence of H 2 S in sulfide spring P. mexicana but not ancestral lineages from nonsulfidic habitats due to convergent adaptations in the primary toxicity target and a major detoxification enzyme. Genome-wide local ancestry analyses indicated that convergent evolution of increased H 2 S tolerance in different populations is likely caused by a combination of selection on standing genetic variation and de novo mutations. On a macroevolutionary scale, H 2 S tolerance in 10 independent lineages of sulfide spring fishes across multiple genera of Poeciliidae is correlated with the convergent modification and expression changes in genes associated with H 2 S toxicity and detoxification. Our results demonstrate that the modification of highly conserved physiological pathways associated with essential mitochondrial processes mediates tolerance to physiochemical stress. In addition, the same pathways, genes, and—in some instances—codons are implicated in H 2 S adaptation in lineages that span 40 million years of evolution. 
    more » « less
  5. Abstract

    Visual sensitivity and body pigmentation are often shaped by both natural selection from the environment and sexual selection from mate choice. One way of quantifying the impact of the environment is by measuring how traits have changed after colonization of a novel habitat. To do this, we studiedPoecilia mexicanapopulations that have repeatedly adapted to extreme sulphidic (H2S‐containing) environments. We measured visual sensitivity using opsin gene expression, as well as body pigmentation, for populations in four independent drainages. Both visual sensitivity and body pigmentation showed significant parallel shifts towards greater medium‐wavelength sensitivity and reflectance in sulphidic populations. Altogether we found that sulphidic habitats select for differences in visual sensitivity and pigmentation. Shifts between habitats may be due to both differences in the water's spectral properties and correlated ecological changes.

     
    more » « less