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Abstract Reconstructions of evolutionary history can be restricted by a lack of high-quality reference genomes. To date, only four of the eight species of bears (family Ursidae) have chromosome-level genome assemblies. Here, we present assemblies for three additional species—the sun, sloth, and Andean bears—and use a whole-genome alignment of all bear species and other carnivores to reconstruct the evolution of Ursidae. Multiple divergence dating approaches suggest that the six Ursine bears likely diversified in the last 5 Ma, but that divergence times within Ursinae are significantly impacted by gene tree heterogeneity. Consistent with this, we observe that nearly 50% of gene trees conflict with our highly supported species tree, a pattern driven by a significant early hybridization event within Ursinae. We also find that the karyotype of Ursinae is largely similar to the ancestral karyotype of all bears twenty million years prior. In contrast to this conservation of structure, dozens of chromosomal fissions and fusions associated with LINE/L1 retrotransposons dramatically restructured the genomes of the giant panda and Andean bear. Finally, we leverage these genomes to identify species-specific evidence for positive selection on genes associated with color, diet, and metabolism. One of these genes, TCPN2, has a role in pigmentation and shows a series of amino acid mutations in the polar bear over the last 0.5 Ma. Collectively, these new genomic resources enable improved reconstruction of the complex evolutionary history of bears and clarify how this enigmatic group diversified. 

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 Habitat transitions have shaped the evolutionary trajectory of many clades. Sea catfishes (Ariidae) have repeatedly undergone ecological transitions, including colonizing freshwaters from marine environments, leading to an adaptive radiation in Australia and New Guinea alongside non-radiating freshwater lineages elsewhere. Here, we generate and analyze one long-read reference genome and 66 short-read whole genome assemblies, in conjunction with genomic data for 54 additional species. We investigate how three major ecological transitions have shaped genomic variation among ariids over their ~ 50 million-year evolutionary history. Our results show that relatively younger freshwater lineages exhibit a higher incidence of positive selection than their more ancient marine counterparts. They also display a larger disparity in body shapes, a trend that correlates with a heightened occurrence of positive selection on genes associated with body size and elongation. Although positive selection in the Australia and New Guinea radiation does not stand out compared to non-radiating lineages overall, selection across the prolactin gene family during the marine-to-freshwater transition suggests that strong osmoregulatory adaptations may have facilitated their colonization and radiation. Our findings underscore the significant role of selection in shaping the genome and organismal traits in response to habitat shifts across macroevolutionary scales. 

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 Hydrogen sulfide is a toxic gas that disrupts numerous biological processes, including energy production in the mitochondria, yet fish in thePoecilia mexicanaspecies complex have independently evolved sulfide tolerance several times. Despite clear evidence for convergence at the phenotypic level in these fishes, it is unclear if the repeated evolution of hydrogen sulfide tolerance is the result of similar genomic changes. To address this gap, we used a targeted capture approach to sequence genes associated with sulfide processes and toxicity from five sulfidic and five nonsulfidic populations in the species complex. By comparing sequence variation in candidate genes to a reference set, we identified similar population structure and differentiation, suggesting that patterns of variation in most genes associated with sulfide processes and toxicity are due to demographic history and not selection. But the presence of tree discordance for a subset of genes suggests that several loci are evolving divergently between ecotypes. We identified two differentiation outlier genes that are associated with sulfide detoxification in the mitochondria that have signatures of selection in all five sulfidic populations. Further investigation into these regions identified long, shared haplotypes among sulfidic populations. Together, these results reveal that selection on standing genetic variation in putatively adaptive genes may be driving phenotypic convergence in this species complex. 

Supergenes can evolve when recombination-suppressing mechanisms like inversions promote co-inheritance of alleles at two or more polymorphic loci that affect a complex trait. Theory shows that such genetic architectures can be favoured under balancing selection or local adaptation in the face of gene flow, but they can also bring costs associated with reduced opportunities for recombination. These costs may in turn be offset by rare ‘gene flux’ between inverted and ancestral haplotypes, with a range of possible outcomes. We aimed to shed light on these processes by investigating the ‘BC supergene’, a large genomic region comprising multiple rearrangements associated with three distinct wing colour morphs inDanaus chrysippus, a butterfly known as the African monarch, African queen and plain tiger. Using whole-genome resequencing data from 174 individuals, we first confirm the effects of BC on wing colour pattern: background melanism is associated with SNPs in the promoter region ofyellow, within an inverted subregion of the supergene, while forewing tip pattern is most likely associated with copy-number variation in a separate subregion of the supergene. We then show that haplotype diversity within the supergene is surprisingly extensive: there are at least six divergent haplotype groups that experience suppressed recombination with respect to each other. Despite high divergence between these haplotype groups, we identify an unexpectedly large number of natural recombinant haplotypes. Several of the inferred crossovers occurred between adjacent inversion ‘modules’, while others occurred within inversions. Furthermore, we show that new haplotype groups have arisen through recombination between two pre-existing ones. Specifically, an allele for dark colouration in the promoter ofyellowhas recombined into distinct haplotype backgrounds on at least two separate occasions. Overall, our findings paint a picture of dynamic evolution of supergene haplotypes, fuelled by incomplete recombination suppression. 

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.