Genomic evidence that blind cavefishes are not wrecks of ancient life

Abstract

Cavefishes often have modified eyes, from small but otherwise functional, to highly degenerate structures embedded in a connective tissue and covered by skin. Darwin assumed that these animals are wrecks of ancient life, but several genomic studies suggests they are not ancient. The most radical dating shift is for populations of a Mexican cavefish, Astyanax mexicanus, that have been recently estimated to be at the most a few tens of thousands years old. Despite having highly degenerate eyes, the eye-specific genes of A. mexicanus have low levels of decay. Other blind cavefishes we have examined so far are even older, but also can be dated to the Pleistocene. Here, we estimated the age of blindness of two additional fish species by the level of decay of eye-specific genes. Many pseudogenes were identified in the amblyopsid Typhlichthys subterraneus, suggesting that blindness evolved a few million years ago. In contrast, the blind cichlid Lamprologus lethops appears to be a new case of very recent and rapid eye regression, which occurred in deep river water, an environment similar to caves. Genome-wide analyses support the hypothesis that blindness in cavefishes is never very ancient, and ranges from the Early Pliocene to Late Pleistocene. Together with the description of hundreds of cavefish species, our results suggest that surface fishes were able to recurrently and rapidly adapt to caves and similar small dark ecosystems but the resulting highly specialized blind species with a limited distribution may be evolutionary dead-ends in a relatively short time.