Divergent selection along ecological gradients can lead to speciation, and replicated speciation events occur when populations of multiple lineages undergo divergence following colonization of similar environments. In such instances, it remains unclear to what extent reproductive isolation evolves via convergent mechanisms at the genomic level due to biases in the types of systems typically used to study convergent evolution. We used a unique system in which three species of poeciliid fishes occur in sympatry in an extremely toxic, hydrogen sulfide (H2S)-rich spring and an adjacent nonsulfidic stream to examine shared patterns of adaptive divergence across multiple levels of biological organization. Despite extremely small spatial scales, we found strong genetic differentiation between populations in sulfidic and nonsulfidic habitats mediated by strong selection against migrants between habitat types. High levels of reproductive isolation were accompanied by convergent patterns of adaptation in morphological and physiological traits, as well as genome-wide patterns of gene expression across all three species. Furthermore, the mitochondrial genomes of each species exhibit shared signatures of selection on key genes involved in H2S toxicity. However, contrary to predictions of speciation theory, analyses of divergence across the nuclear genome neither revealed evidence for clear genomic islands of speciation nor substantial congruence of outlier regions across population pairs. Instead, heterogenous regions of divergence spread across the genome suggest that selection for polygenic physiological adaptations likely facilitated the rapid evolution of high levels of reproductive isolation. Overall, we demonstrate that substantial convergence across multiple levels of biological organization can be mediated by non-convergent modifications at the genomic level. By disentangling environmental variation in natural selection from lineage-specific evolution in this system of highly divergent, yet sympatric lineages, our results emphasize the outsized role of the genomic substrate upon which selection acts in driving convergent evolution at the phenotypic level.

No abstract