A Novel Role for Mc1r in the Parallel Evolution of Depigmentation in Independent Populations of the Cavefish Astyanax mexicanus

Abstract

The evolution of degenerate characteristics remains a poorly understood phenomenon. Only recently has the identification of mutations underlying regressive phenotypes become accessible through the use of genetic analyses. Focusing on the Mexican cave tetra Astyanax mexicanus, we describe, here, an analysis of the brown mutation, which was first described in the literature nearly 40 years ago. This phenotype causes reduced melanin content, decreased melanophore number, and brownish eyes in convergent cave forms of A. mexicanus. Crosses demonstrate non-complementation of the brown phenotype in F2 individuals derived from two independent cave populations: Pachón and the linked Yerbaniz and Japonés caves, indicating the same locus is responsible for reduced pigmentation in these fish. While the brown mutant phenotype arose prior to the fixation of albinism in Pachón cave individuals, it is unclear whether the brown mutation arose before or after the fixation of albinism in the linked Yerbaniz/Japonés caves. Using a QTL approach combined with sequence and functional analyses, we have discovered that two distinct genetic alterations in the coding sequence of the gene Mc1r cause reduced pigmentation associated with the brown mutant phenotype in these caves. Our analysis identifies a novel role for Mc1r in the evolution of degenerative phenotypes in blind Mexican cavefish. Further, the brown phenotype has arisen independently in geographically separate caves, mediated through different mutations of the same gene. This example of parallelism indicates that certain genes are frequent targets of mutation in the repeated evolution of regressive phenotypes in cave-adapted species.

Genes, modules and the evolution of cave fish

“…The complementary restitution then would be brought about by the recombination of different loss-of-function genes in F2 cross hybrids, which derive from different geographically remote cave fish populations that have evolved independently. The phenomenon of varying loss-offunction mutations occurring in the same gene in geographically separate cave populations, but nonetheless causing the same phenotypic effect in them, has also been found for the albino gene as well as for the brown gene (Protas et al, 2007;Gross et al, 2009). In each of these pigment genes, different mutations in separate cave populations cause the same phenotypic defect, namely total or partial loss of melanin.…”

Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism

“…As a result, when species from such clades experience the same selective conditions, they may adapt in genetically and developmentally similar ways (Haldane 1932;Gould 2002;Hoekstra 2006). Recent studies have provided many examples in which parallel phenotypic change in closely related species (or populations of the same species) is caused by similar genetic changes in a wide range of organisms and traits (e.g., Sucena et al 2003;Colosimo et al 2005;Hoekstra et al 2006;Protas et al 2006;Shapiro et al 2006;Whittall et al 2006;Baxter et al 2008;Gross et al 2009;Chan et al 2010; of course, this is not always the case: sometimes convergent phenotypic evolution is accomplished by different genetic changes, even in closely related species [e.g., Hoekstra and Nachman 2003;Wittkopp et al 2003;Hoekstra et al 2006;Kingsley et al 2009] Bossuyt and Milinkovitch 2000;Ruedi and Mayer 2001;Stadelmann et al 2007), and the examples that have been suggested require further examination to assess the extent of species-forspecies matching (Losos 2009). Radiations occurring on different continents usually will be accomplished by distantly related clades that are, for reasons just discussed, likely to diversify in different ways (Pianka 1986;Cadle and Greene 1993;Losos 1994).…”

Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus

“…There is evidence in A. mexicanus that some morphological traits evolved through changes in the same genes in multiple cave populations (9,10). In addition, there is evidence for coevolution of behavioral and morphological traits through the same genetic loci, for example, neuromast number and vibration response (22).…”

“…For example, loss of pigmentation evolved via disruptions in the first step of the melanin synthesis pathway in multiple species of cave organisms (8). Similarly, a decrease in the levels of melanin synthesis arose in multiple cave populations of A. mexicanus through different mutations in the same genes (9,10). In contrast, crosses between multiple cave populations of A. mexicanus result in embryonic hybrid fish with larger, functional eyes, indicating that evolution of this trait is controlled by different genetic loci in different cave populations (2, 11).…”