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1. Evolutionary Rate Shifts in Coding and Regulatory Regions Underpin Repeated Adaptation to Sulfidic Streams in Poeciliid Fishes

   https://doi.org/10.1093/gbe/evae087  

   De-Kayne, Rishi; Perry, Blair W; McGowan, Kerry L; Landers, Jake; Arias-Rodriguez, Lenin; Greenway, Ryan; Rodríguez_Peña, Carlos M; Tobler, Michael; Kelley, Joanna L (May 2024, Genome Biology and Evolution)

   Graham, Allie (Ed.)

   Abstract Adaptation to extreme environments often involves the evolution of dramatic physiological changes. To better understand how organisms evolve these complex phenotypic changes, the repeatability and predictability of evolution, and possible constraints on adapting to an extreme environment, it is important to understand how adaptive variation has evolved. Poeciliid fishes represent a particularly fruitful study system for investigations of adaptation to extreme environments due to their repeated colonization of toxic hydrogen sulfide–rich springs across multiple species within the clade. Previous investigations have highlighted changes in the physiology and gene expression in specific species that are thought to facilitate adaptation to hydrogen sulfide–rich springs. However, the presence of adaptive nucleotide variation in coding and regulatory regions and the degree to which convergent evolution has shaped the genomic regions underpinning sulfide tolerance across taxa are unknown. By sampling across seven independent lineages in which nonsulfidic lineages have colonized and adapted to sulfide springs, we reveal signatures of shared evolutionary rate shifts across the genome. We found evidence of genes, promoters, and putative enhancer regions associated with both increased and decreased convergent evolutionary rate shifts in hydrogen sulfide–adapted lineages. Our analysis highlights convergent evolutionary rate shifts in sulfidic lineages associated with the modulation of endogenous hydrogen sulfide production and hydrogen sulfide detoxification. We also found that regions with shifted evolutionary rates in sulfide spring fishes more often exhibited convergent shifts in either the coding region or the regulatory sequence of a given gene, rather than both. 

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2. Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide–rich springs

   https://doi.org/10.1073/pnas.2014929118  

   Kelley, Joanna L.; Tobler, Michael; Beck, Daniel; Sadler-Riggleman, Ingrid; Quackenbush, Corey R.; Arias Rodriguez, Lenin; Skinner, Michael K. (June 2021, Proceedings of the National Academy of Sciences)

   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. 

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3. Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments

   https://doi.org/10.1073/pnas.2004223117  

   Greenway, Ryan; Barts, Nick; Henpita, Chathurika; Brown, Anthony P.; Arias Rodriguez, Lenin; Rodríguez Peña, Carlos M.; Arndt, Sabine; Lau, Gigi Y.; Murphy, Michael P.; Wu, Lei; et al (July 2020, Proceedings of the National Academy of Sciences)

   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. 

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4. Nascent transcription reveals regulatory changes in extremophile fishes inhabiting hydrogen sulfide-rich environments

   https://doi.org/10.1098/rspb.2024.0412  

   Perry, Blair W; McGowan, Kerry L; Arias-Rodriguez, Lenin; Duttke, Sascha H; Tobler, Michael; Kelley, Joanna L (June 2024, Proceedings of the Royal Society B: Biological Sciences)

   Regulating transcription allows organisms to respond to their environment, both within a single generation (plasticity) and across generations (adaptation). We examined transcriptional differences in gill tissues of fishes in thePoecilia mexicanaspecies complex (family Poeciliidae), which have colonized toxic springs rich in hydrogen sulfide (H₂S) in southern Mexico. There are gene expression differences between sulfidic and non-sulfidic populations, yet regulatory mechanisms mediating this gene expression variation remain poorly studied. We combined capped-small RNA sequencing (csRNA-seq), which captures actively transcribed (i.e. nascent) transcripts, and messenger RNA sequencing (mRNA-seq) to examine how variation in transcription, enhancer activity, and associated transcription factor binding sites may facilitate adaptation to extreme environments. csRNA-seq revealed thousands of differentially initiated transcripts between sulfidic and non-sulfidic populations, many of which are involved in H₂S detoxification and response. Analyses of transcription factor binding sites in promoter and putative enhancer csRNA-seq peaks identified a suite of transcription factors likely involved in regulating H₂S-specific shifts in gene expression, including several key transcription factors known to respond to hypoxia. Our findings uncover a complex interplay of regulatory processes that reflect the divergence of extremophile populations ofP. mexicanafrom their non-sulfidic ancestors and suggest shared responses among evolutionarily independent lineages. 

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5. Phenotypic differentiation in populations of a gladiator tree frog: environment, genetic drift and sexual selection

   https://doi.org/10.1093/biolinnean/blad028  

   Nali, Renato C; Zamudio, Kelly R; Prado, Cynthia P (June 2023, Biological Journal of the Linnean Society)

   Abstract Phenotypic differentiation among animal populations is common, yet few studies have simultaneously examined the adaptive and neutral mechanisms behind it. Such evolutionary processes become more relevant in species with complex behaviours that undergo global and local selective pressures throughout their geographical range. Here we measured and compared morphological and acoustic variation across the distribution range of a Neotropical gladiator tree frog that shows elaborate reproduction (territoriality, complex courtship and female choice). We then incorporated molecular and landscape data to examine the roles of sexual selection, genetic drift and acoustic adaptation to the environment in call differentiation, i.e. the acoustic adaptation hypothesis (AAH). We found that calls varied more than morphology among populations, but differences in calls or morphological traits were not explained by genetic differentiation. We found no evidence for the AAH, but a significant relationship in the opposite direction regarding call frequencies suggests an indirect role of sexual selection. Differentiation on call traits that are associated with individual discrimination and/or female attraction also corroborated an important role of sexual selection. We show that multitrait and multimechanism approaches can elucidate intricate processes leading to phenotypic variation among individuals and populations. We emphasize that studies of species with complex reproductive behaviours across their range may provide insights into different selective pressures leading to phenotypic differentiation. 

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