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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. 

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. 

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 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. 

Salinity gradients act as strong environmental barriers that limit the distribution of aquatic organisms. Changes in gene expression associated with transitions between freshwater and saltwater environments can provide insights into organismal responses to variation in salinity. We used RNA-sequencing (RNA-seq) to investigate genome-wide variation in gene expression between a hypersaline population and a freshwater population of the livebearing fish speciesLimia perugiae(Poeciliidae). Our analyses of gill gene expression revealed potential molecular mechanisms underlying salinity tolerance in this species, including the enrichment of genes involved in ion transport, maintenance of chemical homeostasis, and cell signaling in the hypersaline population. We also found differences in gene expression patterns associated with cell-cycle and protein-folding processes between the hypersaline and freshwaterL.perugiae. Bidirectional freshwater-saltwater transitions have occurred repeatedly during the diversification of fishes, allowing for broad-scale examination of repeatable patterns in evolution. Therefore, we compared transcriptomic variation inL.perugiaewith other teleosts that have made freshwater-saltwater transitions to test for convergence in gene expression. Among the four distantly related population pairs from high- and low-salinity environments that we included in our analysis, we found only ten shared differentially expressed genes, indicating little evidence for convergence. However, we found that differentially expressed genes shared among three or more lineages were functionally enriched for ion transport and immune functioning. Overall, our results—in conjunction with other recent studies—suggest that different genes are involved in salinity transitions across disparate lineages of teleost fishes. 

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. 

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.