Ecology drives the degree of convergence in the gene expression of extremophile fishes

Abstract Convergent evolution is common and a testament to the repeatability of evolution. Still, non-convergence is also widespread, and a major question is whether idiosyncratic, lineage-specific changes are reflective of chance events inherent to evolutionary processes, or whether they are influenced by deterministic genetic or ecological factors. To address this question, we quantified the degree of convergence in gene expression across lineages of livebearing fishes (Poeciliidae) that span 40 million years of divergence and have colonized toxic, hydrogen-sulfide-rich springs. We asked whether the degree of convergence across lineage pairs was related to their phylogenetic relatedness and the ecological similarity of their habitats. Using phylogenetic comparative analyses, we showed that the degree of convergence in gene expression was variable across lineage pairs. While closely related lineages did not exhibit higher degrees of convergence than distantly related ones, we uncovered a strong relationship between degree of convergence and the ecological similarity among lineages. These results suggest that variation in environmental conditions that is often overlooked in simplified descriptions of habitat differences can play an important role in shaping adaptive evolution. Our study highlights the importance of multivariate approaches that capture the complexities of selective regimes and organismal responses when assessing the repeatability of evolution.