Convergent evolution of conserved mitochondrial pathways underlies repeated adaptation to extreme environments

Abstract

Extreme environments test the limits of life. Still, some organisms thrive in harsh conditions, begging the question whether the repeated colonization of extreme environments is facilitated by predictable and repeatable evolutionary innovations. We identified the mechanistic basis underlying convergent evolution of tolerance to hydrogen sulfide (H₂S)—a potent toxicant that impairs mitochondrial function—across evolutionarily independent lineages of a fish (Poecilia mexicana, Poeciliidae) from H₂S-rich freshwater springs. We found that mitochondrial function is maintained in the presence of H₂S in sulfide spring P. mexicana, but not ancestral lineages in adjacent nonsulfidic habitats, due to convergent adaptations in both the primary toxicity target and a major detoxification enzyme. Additionally, we show that H₂S tolerance in 10 independent lineages of sulfide spring fishes across multiple genera of Poeciliidae is mediated by convergent modification and expression changes of genes associated with H₂S toxicity and detoxification. Our results demonstrate that the repeated modification of highly conserved physiological pathways associated with essential mitochondrial processes enabled the colonization of novel environments.