Massive Expansion of Bitter Taste Receptors in Blind Cavefish, Astyanax mexicanus

A sensory deficit both at the individual and at the species level can be compensated by increased acuity in other senses. The loss of vision in blind cavefish, Astyanax mexicanus, appears to be partially counterbalanced by enhanced chemosensory perception. Whether such improvement also involves adaptive changes in chemosensory receptor repertoires was unknown. The typical bitter taste receptor repertoire of teleost fish is reported as 3-5 genes, much smaller than that of many terrestrial species. Interestingly, several fish species, for example, mudskipper, have evolved a terrestrial lifestyle, but again it was unknown, whether this change in habitat is reflected in the size of gustatory receptor repertoires. We have searched the genomes of 15 fish species and performed a thorough phylogenetic analysis to delineate their bitter taste receptor repertoires. We report no adaptation for 4 mudskipper species, which exhibit 3-4 bitter taste receptor genes, and thus a typical teleost repertoire, shaped by few gene losses and minor gene duplications from an ancestral repertoire of 4 genes. However, and in sharp contrast to all other teleost fish species analyzed, blind cavefish possess more than 20 intact bitter taste receptors and several pseudogenes, rivaling the complexity of the human bitter taste receptor repertoire. The gene duplications giving rise to the current cavefish bitter taste receptor repertoire appear to have occurred well before the loss of vision, consistent with this increase in repertoire size constituting a preadaptive trait that conceivably could compensate to some extent for the lack of visual cues.