Gross JB, Borowsky R, Tabin CJ. A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet 5: e1000326

Department of Genetics, Harvard Medical School, Boston, Massachusetts, United States of America.
PLoS Genetics (Impact Factor: 7.53). 02/2009; 5(1):e1000326. DOI: 10.1371/journal.pgen.1000326
Source: PubMed


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 F(2) 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.

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    • "There are no sequence differences in the Mc1r coding region of Tinaja or Chica compared to surface-dwelling fish based on a prior analysis in which the Mc1r open reading frame was sequenced and compared across 13 populations (Gross et al. 2009). Previous functional analyses of Mc1r, in which mRNA transcripts were abrogated using morpholino knock-down approaches , demonstrated that reduced levels of Mc1r recapitulate the brownish eyes and reduced melanic content found in the classic brown phenotype (Gross et al. 2009). Thus, the functional role of Mc1r, combined with the divergent expression patterns we report here, may explain the parallel evolution of reduced pigmentation in wild cavefish. "
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    ABSTRACT: Diverse changes in coloration across distant taxa are mediated through alterations in certain highly conserved pigmentation genes. Among these genes, Mc1r is a frequent target for mutation, and many documented alterations involve coding sequence changes. We investigated whether regulatory mutations in Mc1r may also contribute to pigmentation loss in the blind Mexican cavefish, Astyanax mexicanus. This species comprises multiple independent cave populations that have evolved reduced (or absent) melanic pigmentation as a consequence of living in darkness for millions of generations. Among the most salient cave-associated traits, complete absence (albinism) or reduced levels of pigmentation (brown) have long been the focus of degenerative pigmentation research in Astyanax. These two Mendelian traits have been linked to specific coding mutations in Oca2 (albinism) and Mc1r (brown). However, four of the seven caves harboring the brown phenotype exhibit unaffected coding sequences compared to surface fish. Thus, diverse genetic changes involving the same genes likely impact reduced pigmentation among cavefish populations. Using both sequence and expression analyses, we show that certain cave-dwelling populations harboring the brown mutation have substantial alterations to the putative Mc1r cis-regulatory region. Several of these sequence mutations in the Mc1r 5' region were present across multiple, independent cave populations. This study suggests that pigmentation reduction in Astyanax cavefish evolves through a combination of both coding and cis-regulatory mutations. Moreover, this study represents one of the first attempts to identify regulatory alterations linked to regressive changes in cave-dwelling populations of A. mexicanus.
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    • "& Devon E. Pearse 1 Institute of Marine Sciences, University of California, Santa Cruz, Santa Cruz, CA 95060, USA 2 Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 110 Shaffer Road, Santa Cruz, CA 95060, USA Mundy et al. 2004; Colosimo et al. 2005; Gross et al. 2009; Hohenlohe et al. 2012; Miller et al. 2012; Protejo-Garcia et al. 2013; Pearse et al. 2014 "
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    ABSTRACT: Parallel adaptive divergence of migratory and reproductive behavior can occur in multiple populations when similar selection is acting on these traits. Timing of migration, sexual maturity, and reproduction can have major impacts on the dynamics and viability of a population. Life-history variation in steelhead, Oncorhynchus mykiss, including variation in anadromous run timing, reproductive maturity, and spawn timing, represents an important aspect of their biology and adaptation to local habitats. Here we present a genetic analysis of naturally spawning steelhead to evaluate the genetic relationships and ancestry of summer- and winter-run reproductive ecotypes from multiple river basins in Oregon and Northern California. We infer the phylogeographic relationships among populations of both summer- and winter-run steelhead ecotypes using 12 microsatellite loci and 90 single nucleotide polymorphisms. Phylogenetic trees and analysis of molecular genetic variance revealed that pairs of phenotypically and genetically distinct reproductive ecotypes within rivers were each other’s closest relatives. Isolation by distance was also observed, confirming that genetic relatedness was strongly associated with geographic distance, and indicating limited gene flow among river basins. These patterns support the hypothesis that the summer-run steelhead ecotype has repeatedly evolved through parallel evolution in multiple river basins. Our results, together with further investigations of the underlying molecular basis for the divergence of winter- and summer-run steelhead life-history traits, inform management efforts for these ecotypes and improve our understanding of the role of adaptive genetic variation in conservation. © 2015 Springer Science+Business Media Dordrecht (outside the USA)
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    • "However, there are additional cases where shared phenotypes in geographically disparate populations arise through different mutations at a given locus (e.g. Gross et al., 2009; Chan et al., 2010; reviewed by Martin & Orgogozo, 2013) or through mutations at different underlying loci (Steiner et al., 2009; Samis et al., 2012). Characterizing the genomic and geographical context of parallel phenotypic evolution can provide clues about the nature of evolutionary constraint and the mechanisms underlying adaptation. "
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    ABSTRACT: Variation in cyanogenesis (hydrogen cyanide release following tissue damage) was first noted in populations of white clover more than a century ago, and subsequent decades of research have established this system as a classic example of an adaptive chemical defence polymorphism. Here, we document polymorphisms for cyanogenic components in several relatives of white clover, and we determine the molecular basis of this trans-specific adaptive variation. One hundred and thirty-nine plants, representing 13 of the 14 species within Trifolium section Trifoliastrum, plus additional species across the genus, were assayed for cyanogenic components (cyanogenic glucosides and their hydrolysing enzyme, linamarase) and for the presence of underlying cyanogenesis genes (CYP79D15 and Li, respectively). One or both cyanogenic components were detected in seven species, all within section Trifoliastrum; polymorphisms for the presence/absence (PA) of components were detected in six species. In a pattern that parallels our previous findings for white clover, all observed biochemical polymorphisms correspond to gene PA polymorphisms at CYP79D15 and Li. Relationships of DNA sequence haplotypes at the cyanogenesis loci and flanking genomic regions suggest independent evolution of gene deletions within species. This study thus provides evidence for the parallel evolution of adaptive biochemical polymorphisms through recurrent gene deletions in multiple species.
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