A common mechanism and multiple advantages of pigment loss underlie the convergent evolution of albinism in cave animals

The loss of pigmentation is a hallmark adaptation of cave-dwelling animals but the underlying mechanisms are poorly understood. This study investigates the cellular and biochemical basis of albinism, the loss of melanin pigment, which convergently evolved across a wide range of cave animals. Is albinism caused by the interruption of pigment synthesis or elimination of the pigment cell lineage? The results suggest that albinism evolved by a common mechanism, a block in the first step of the melanin biosynthesis pathway, the conversion of L-tyrosine to L-DOPA, in diverse albino cave animals ranging from annelids and mollusks to vertebrates. Pigment cells are conserved in all tested albino cave species and distributed in patterns resembling pigmentation in their close surface relatives. The cells capable of melanin synthesis when provided with L-DOPA substrate were detected at the sites of injuries in a cave annelid, cave mollusk, and cave teleost, suggesting roles in innate immunity during tissue repair, which may explain why pigment cells are conserved despite the loss of pigment production. Next, we focused on the longstanding issue of the evolutionary forces involved in the regression of pigmentation in cave animals and explored hypotheses of why losing pigmentation might be adaptive in cave environments. First, we tested the hypothesis that pigment regression may conserve energy, which is important for survival in the food-limited cave environment. Our results indicate that melanin synthesis has a marked energetic cost in the cavefish, Astyanax mexicanus. Lastly, we show that the disruption of melanin synthesis at its first biosynthetic step is correlated with increased dopamine levels in multiple depigmented cavefish populations, including populations that evolved albinism independently. This result supports a widespread tradeoff between the melanin and catecholamine synthesis pathways in A. mexicanus. We conclude that the interruption of the conversion of L-tyrosine to L-DOPA in the synthesis of melanin confers multiple advantages that could serve as targets of natural selection, supporting an adaptive hypothesis for the evolution of albinism in cave animals.