Regressive Evolution of Pigmentation in the Cavefish Astyanax

Abstract

Many cave animals are colorless due to loss of pigment cells. Here, we review recent progress on how and why pigmentation has disappeared inAstyanax mexicanus, a single teleost species with conspecific surface-dwelling (surface fish) and many different cave-dwelling (cavefish) forms. During surface fish development, migratory neural crest cells form three types of pigment cells: silver iridophores, orange xanthophores, and black melanophores. Cavefish have eliminated or substantially reduced their complement of melanophores and exhibit albinism, loss of the capacity to synthesize melanin. Cell tracing, immunolocalization, and neural tube explant cultures show that cavefish have retained a colorless pre-melanophore (melanoblast) lineage derived from the neural crest. Thus, the cavefish neural crest produces melanoblasts that migrate normally but are blocked in differentiation and show defective melanogenesis. Cavefish melanoblasts can convert exogenous L-DOPA into melanin and therefore have active tyrosinase, the key enzyme in melanogenesis. In contrast, cavefish melanoblasts are unable to convert L-tyrosine to L-DOPA (and melanin), although this reaction is also catalyzed by tyrosinase. Thus, cavefish are tyrosinase-positive albinos that have a deficiency in L-tyrosine transport or utilization within the melanosome, the organelle in which melanin is synthesized. At least five different types ofAstyanaxcavefish show the same defect in melanogenesis. Genetic analysis shows that cavefish albinism is caused by loss of function mutations in a single gene,p/oca2, which encodes a large protein that probably spans the melanosome membrane. Different deletions in thep/oca2 protein-coding region are responsible for loss of function in at least two different cavefish populations, suggesting that albinism evolved by convergence. Based on current understanding of the genetic basis of albinism, we discuss potential mechanisms for regressive evolution of cavefish pigmentation.