engleski

Convergent Evolution of Albinism in Cave Animals: A Defect in the First Step of Melanin Biosynthesis in Troglomorphic Fishes and Insects

Cave adapted animals are often characterized by the absence of melanin pigment, a condition known as albinism. Here we ask whether albinism has evolved by the same or different changes in the melanin biosynthesis pathway in two diverse lineages of cave adapted animals, fishes (teleosts) and insects (planthoppers). In Astyanax mexicanus cavefish, albinism is caused by mutations in the oca2 gene, which acts during the initial step of melanin biosynthesis: the conversion of L-tyrosine to L-DOPA. We have developed a functional assay for detecting the position of changes in melanin biosynthesis by supplying exogenous substrates, such as L-tyrosine or L-DOPA, to lightly fixed specimens, and subsequently detecting melanin as deposits of black pigment. Because the melanin synthesis pathway is conserved across wide phylogenetic distances, this assay can assess whether the initial steps of melanin biosynthesis are functional in diverse cave animals. For example, black pigment can be rescued in independently evolved populations of A. mexicanus cavefish by supplying L-DOPA but not L-tyrosine substrate, demonstrating the conservation of functional tyrosinase in the pathway and a convergent defect at its first step. The rescue is blocked by prior treatment of the specimens with high temperature or co-assay with phenylthiourea, an inhibitor of tyrosinase, indicating that it is an enzyme-catalyzed reaction. Similar results were obtained with two other albino cavefish that evolved albinism separately from A. mexicanus, Typhlichthys subterraneous and Amblyopsis spelaea, but not in some surface-dwelling albino fishes, which may have changed a downstream step in the pathway. To investigate the phylogenetic scope of this convergence, we performed similar assays on independently evolved albino cixiid planthoppers from limestone caves in Mljet and Biokovo, Croatia (unidentified species) and lava tubes in Hawaii (Oliarus polyphemus). In each case, supplying exogenous L-DOPA or dopamine (another initial substrate in a parallel melanogenesis pathway in insects) but not L-tyrosine produced black pigment, implying a defect also occurs in the first step in the melanin biosynthesis pathway in these organisms. Therefore, albinism has evolved via convergent evolution by interfering with the same initial step of the melanin biosynthesis pathway in both cave-adapted fishes and insects. We are currently investigating the possibility that this convergence is even broader than described here by conducting the substrate assays in many different albino invertebrate species. In addition, we are developing testable hypotheses to explain the potential adaptive significance of repeatedly blocking melanin biosynthesis at its first step in cave-adapted animals.

albinism; melanin synthesis; cavefish; cave insects; OCA2

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