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

   https://doi.org/10.1111/mec.14360  

   Passow, Courtney N. ; Henpita, Chathurika ; Shaw, Jennifer H. ; Quackenbush, Corey R. ; Warren, Wesley C. ; Schartl, Manfred ; Arias‐Rodriguez, Lenin ; Kelley, Joanna L. ; Tobler, Michael ( October 2017 , Molecular Ecology)

   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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3. microRNA expression variation as a potential molecular mechanism contributing to adaptation to hydrogen sulphide

   https://doi.org/10.1111/jeb.13727  

   Kelley, Joanna L. ; Desvignes, Thomas ; McGowan, Kerry L. ; Perez, Marcos ; Rodriguez, Lenin Arias ; Brown, Anthony P. ; Culumber, Zach ; Tobler, Michael ( November 2020 , Journal of Evolutionary Biology)

   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.

    

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4. Discerning structure versus speciation in phylogeographic analysis of Seepage Salamanders ( Desmognathus aeneus ) using demography, environment, geography, and phenotype

   https://doi.org/10.1111/mec.17219  

   Pyron, R. Alexander ; Kakkera, Anvith ; Beamer, David A. ; O'Connell, Kyle A. ( November 2023 , Molecular Ecology)

   Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long‐term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure” versus “species” when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species‐delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

    

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5. Sexual selection and the ascent of women: Mate choice research since Darwin

   https://doi.org/10.1126/science.abi6308  

   Rosenthal, Gil G. ; Ryan, Michael J. ( January 2022 , Science)

   BACKGROUND Charles Darwin’s  Descent of Man, and Selection in Relation to Sex  tackled the two main controversies arising from the Origin of Species:  the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCE 

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