Toxic hydrogen sulphide shapes brain anatomy: a comparative study of sulphide‐adapted ecotypes in the Poecilia mexicana complex

The teleost brain is an energetically costly organ, which raises the question of how brain anatomy is shaped by divergent ecological factors in contrasting (extreme/resource-limited vs. benign) environments. A previous study compared different ecotypes of the teleost Poecilia mexicana in the Tacotalpa drainage system and found that cave fish had a smaller eye diameter, a smaller optic tectum and larger telencephalic lobes relative to ancestral surface-dwelling fish. Smaller eyes and a smaller optic tectum but larger telencephalic lobes were also found in fish from a sulphidic surface habitat near one of the caves, which the authors hypothesized to result from limited vision in turbid sulphide waters. In this study, we tested if repeated transitions along a replicated, natural toxicity gradient result in repeated (‘convergent’) anatomical changes of the teleost brain. We compared ecotypes in the P. mexicana species complex that have independently evolved increased tolerance to hydrogen sulphide (H2S) in three river drainages in southern Mexico, including a phylogenetically old H2S-adapted form (P. sulphuraria) and two P. mexicana ecotypes that represent earlier stages of adaptation to H2S. All H2S-adapted ecotypes exhibited smaller eyes, a smaller optic tectum volume and a smaller brain volume, but larger corpora cerebelli and hypothalamic volume than fish from non-sulphidic habitats. Drainage-specific effects were found for the telencephalic lobes, the total brain and eye size, as sexes responded differently to the presence of H2S depending on the drainage of origin. Turbidity and toxicity in sulphidic habitats may explain patterns of brain size divergence similar in direction (but not degree) to those observed in cave ecotypes. Hence, variation in brain anatomy reflects major ecological differences, and repeated ecological gradients can result in convergent differences in brain anatomy. Nonetheless, some unique patterns of brain differentiation suggest as yet unidentified differences in selection regimes between different sulphidic springs.