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ABSTRACT Organisms inhabiting extreme environments must tolerate a variety of physiochemical stressors. In some cases, host‐associated microbial communities facilitate the survival of their hosts in extreme environments, but extremophile symbioses have not been identified in vertebrates. We used 16S rRNA amplicon sequencing to investigate commonalities and differences in the gut bacterial communities of livebearing fishes (Poecilia mexicanaspecies complex, Poeciliidae) that have repeatedly colonised toxic sulfide streams in southern Mexico. We found shared gut microbial taxa across habitat types and drainages but also differences in the microbiomes between sulfidic and nonsulfidic populations, both in terms of patterns of diversity and community composition. Most importantly, we documented convergent changes in microbiome composition across evolutionarily independent sulfide spring lineages. These patterns were consistent when we analysed the gut microbiomes as well as primarily host‐associated microbiomes that excluded taxa that are commonly found in the environment. Our analyses also revealed several microbial taxa associated with sulfide spring coloniation that have previously been implicated in symbioses and may influence the host's tolerance to the extreme environmental conditions. Our study sheds light on how shared environmental pressures can give rise to convergent host‐microbiome associations in fishes, and it provides a foundation for investigating the role of host‐microbiome interactions in vertebrate adaptation to extreme environments. 

Abstract Multiple lineages in the family Poeciliidae have independently adapted to hydrogen-sulfide-rich springs. The independent colonizations of such springs mean that there are naturally replicated lineages that provide a powerful model for studying adaptation and convergent evolution. However, there are limited genomic resources for many genera and species across Poeciliidae. Here, we present six high-quality, chromosome-level, annotated genome assemblies for Poecilia and Gambusia populations, five of which are the first for the species or ecotype, and the remaining assembly improved the current reference genome contiguity by more than 100-fold. Using these new assemblies, we compare repeat content and model historical changes in effective population size. 

Abstract Phenotypic variation is common along environmental gradients, but it is often not known to what extent it results from genetic differentiation between populations or phenotypic plasticity. We studied populations of a livebearing fish that have colonized streams rich in toxic hydrogen sulphide (H2S). There is strong phenotypic differentiation between adjacent sulphidic and non-sulphidic populations. In this study, we varied food availability to pregnant mothers from different populations to induce maternal effects, a form of plasticity, and repeatedly measured life-history and behavioural traits throughout the ontogeny of the offspring. Genetic differentiation affected most of the traits we measured, in that sulphidic offspring tended to be born larger, mature later, have lower burst swimming performance, be more exploratory, and feed less effectively. In contrast, maternal effects impacted few traits and at a smaller magnitude, although offspring from poorly provisioned mothers tended to be born larger and be more exploratory. Population differences and maternal effects (when both were present) acted additively, and there was no evidence for population differences in plasticity. Overall, our study suggests that phenotypic divergence between these populations in nature is caused primarily by genetic differentiation and that plasticity mediated by maternal effects accentuates but does not cause differences between populations. 

Abstract Animal genitalia evolve rapidly because of coevolution between male and female traits. However, how the ecological context in which mating occurs might modulate the evolution of genital traits remains poorly understood. We investigated how a change in the sensory environment (the absence of light upon cave colonization) impacted the expression of genital traits in a live-bearing fish, Poecilia mexicana (Poeciliidae), with populations in adjacent cave and surface habitats. Quantifying characteristics of the female urogenital aperture and the male gonopodium (a modified anal fin used for copulation), we found significant differences in genital traits of both sexes. Females from cave populations exhibited larger and more rounded genitalia. Males from cave populations exhibited a significantly enlarged palp, a fleshy gonopodial appendage that has been hypothesized to have sensory functions. Our results suggest that genital traits can diverge rapidly among closely related populations exposed to different environmental conditions. The absence of light could impact genital evolution directly, if some genital structures have sensory functions that compensate for the lack of visual information during copulation, or indirectly, if the absence of light impacts dynamics of sexual conflict or cryptic female choice that arise through the interaction between the sexes. 

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. 

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. 

Abstract Our understanding of the mechanisms mediating the resilience of organisms to environmental change remains lacking. Heavy metals negatively affect processes at all biological scales, yet organisms inhabiting contaminated environments must maintain homeostasis to survive. Tar Creek in Oklahoma, USA, contains high concentrations of heavy metals and an abundance of Western mosquitofish (Gambusia affinis), though several fish species persist at lower frequency. To test hypotheses about the mechanisms mediating the persistence and abundance of mosquitofish in Tar Creek, we integrated ionomic data from seven resident fish species and transcriptomic data from mosquitofish. We predicted that mosquitofish minimize uptake of heavy metals more than other Tar Creek fish inhabitants and induce transcriptional responses to detoxify metals that enter the body, allowing them to persist in Tar Creek at higher density than species that may lack these responses. Tar Creek populations of all seven fish species accumulated heavy metals, suggesting mosquitofish cannot block uptake more efficiently than other species. We found population‐level gene expression changes between mosquitofish in Tar Creek and nearby unpolluted sites. Gene expression differences primarily occurred in the gill, where we found upregulation of genes involved with lowering transfer of metal ions from the blood into cells and mitigating free radicals. However, many differentially expressed genes were not in known metal response pathways, suggesting multifarious selective regimes and/or previously undocumented pathways could impact tolerance in mosquitofish. Our systems‐level study identified well characterized and putatively new mechanisms that enable mosquitofish to inhabit heavy metal‐contaminated environments. 

Abstract Natural selection drives the evolution of traits to optimize organismal performance, but optimization of one aspect of performance can influence other aspects of performance. Here, we asked how phenotypic variation between locally adapted fish populations affects locomotion and ventilation, testing for functional trade‐offs and trait–performance correlations. Specifically, we investigated two populations of livebearing fish (Poecilia mexicana) that inhabit distinct habitat types (hydrogen‐sulphide‐rich springs and adjacent nonsulphidic streams). For each individual, we quantified different metrics of burst swimming during simulated predator attacks, steady swimming and gill ventilation. Coinciding with predictions, we documented significant population differences in all aspects of performance, with fish from sulphidic habitats exhibiting higher steady swimming performance and higher ventilation capacity, but slower burst swimming. There was a significant functional trade‐off between steady and burst swimming, but not between different aspects of locomotion and ventilation. Although our findings about population differences in locomotion performance largely parallel the results from previous studies, we provide novel insights about how morphological variation might impact ventilation and ultimately oxygen acquisition. Overall, our analyses provided insights into the functional consequences of previously documented phenotypic variation, which will help to disentangle the effects of different sources of selection that may coincide along complex environmental gradients. 

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. 

Asexual species, despite lacking recombination, can evolve in response to environmental changes and influence the evolutionary trajectory of coexisting sexual species. Gynogenesis, where asexual females rely on sperm from males of a different species, offers a unique perspective on the eco-evolutionary dynamics between asexual females and their sexual hosts. The Amazon molly,Poecilia formosa, is a gynogenetic species that primarily uses sperm from two sympatric sexual species: the sailfin molly (P. latipinna) and the Atlantic molly (P. mexicana). To understand shape variation in an asexual species relative to their sexual hosts, we analysed shape variation among wild Amazon mollies and their sexual hosts. We tested three hypotheses: (i) Amazon mollies mimic their sexual hosts to enhance mating opportunities (sexual mimicry hypothesis); (ii) ecological interactions or male mate choice drive morphological divergence (character displacement hypothesis); and (iii) Amazon mollies exhibit random shape variation due to their asexual nature (null hypothesis). Our findings revealed significant shape variation in Amazon mollies, which differ from their sexual hosts in a host-specific manner (e.g. Amazon mollies withP. latipinnaresembleP. mexicanaand vice versa), supporting character displacement at the interspecific level in a sexual–asexual system.