The spatiotemporal and genetic architecture of extraoral taste buds in Astyanax cavefish.

Intense environmental pressures can yield both regressive and constructive traits through complex evolutionary mechanisms. Although regression is well-studied, the biological bases of constructive features are less well understood. Cave-dwelling Astyanax fish harbor prolific extraoral taste buds on their heads, which are absent in conspecific surface-dwellers. Here, we present novel ontogenetic data demonstrating extraoral taste buds appear gradually and late in life history. This appearance is similar but non-identical in different cavefish populations, where patterning has evolved to permit taste bud re-specification across the endoderm-ectoderm germ layer boundary. Quantitative genetic analyses revealed that spatially distinct taste buds on the head are primarily mediated by two different cave-dominant loci. While the precise function of this late expansion on to the head is unknown, the appearance of extraoral taste buds coincides with a dietary shift from live-foods to bat guano, suggesting an adaptive mechanism to detect nutrition in food-starved caves. This work provides fundamental insight to a constructive evolutionary feature, arising late in life history, promising a new window into unresolved features of vertebrate sensory organ development.