cis-Regulatory Changes in Kit Ligand Expression and Parallel Evolution of Pigmentation in Sticklebacks and Humans

HHMI and Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Cell (Impact Factor: 32.24). 01/2008; 131(6):1179-89. DOI: 10.1016/j.cell.2007.10.055
Source: PubMed

ABSTRACT Dramatic pigmentation changes have evolved within most vertebrate groups, including fish and humans. Here we use genetic crosses in sticklebacks to investigate the parallel origin of pigmentation changes in natural populations. High-resolution mapping and expression experiments show that light gills and light ventrums map to a divergent regulatory allele of the Kit ligand (Kitlg) gene. The divergent allele reduces expression in gill and skin tissue and is shared by multiple derived freshwater populations with reduced pigmentation. In humans, Europeans and East Asians also share derived alleles at the KITLG locus. Strong signatures of selection map to regulatory regions surrounding the gene, and admixture mapping shows that the KITLG genomic region has a significant effect on human skin color. These experiments suggest that regulatory changes in Kitlg contribute to natural variation in vertebrate pigmentation, and that similar genetic mechanisms may underlie rapid evolutionary change in fish and humans.

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Available from: Dolph Schluter, Sep 26, 2015
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    • "The revised genome assembly provides a more accurate understanding of the structure of the stickleback genome, which should aid efforts to map genes controlling stickleback phenotypes and understand genomic dynamics during stickleback evolution. The genetic mapping of distinct QTL controlling gill raker length in two crosses illustrates that, in contrast to several prominent cases in sticklebacks (Chan et al. 2010; Colosimo et al. 2005; Miller et al. 2007 "
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    ABSTRACT: Marine populations of the threespine stickleback (Gasterosteus aculeatus) have repeatedly colonized and rapidly adapted to freshwater habitats, providing a powerful system to map the genetic architecture of evolved traits. Here we developed and applied a binned Genotyping-by-Sequencing (GBS) method to build dense genome-wide linkage maps of sticklebacks, using two large marine by freshwater F2 crosses of over 350 fish each. The resulting linkage maps significantly improve the genome assembly by anchoring 78 new scaffolds to chromosomes, reorienting 40 scaffolds, and rearranging scaffolds in 4 locations. In the revised genome assembly, 94.6% of the assembly was anchored to a chromosome. To assess linkage map quality, we mapped quantitative trait loci (QTL) controlling lateral plate number, which mapped as expected to a 200 kilobase genomic region containing Ectodysplasin, as well as a chromosome 7 QTL overlapping a previously identified modifier QTL. Finally, we mapped eight QTL controlling convergently evolved reductions in gill raker length in the two crosses, which revealed that this classic adaptive trait has a surprisingly modular and non-parallel genetic basis. Copyright © 2015 Author et al.
    G3-Genes Genomes Genetics 06/2015; 5(7). DOI:10.1534/g3.115.017905 · 3.20 Impact Factor
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    • "Melanocytes are the only chromatophore type found within birds and mammals (Mills and Patterson, 2009), determining the color of feathers, furs, and skin (Lin and Fisher, 2007). The diversity of pigment pattern found within higher vertebrates is generated due to different contributions of the 2 types of melanin (Mills and Patterson, 2009), mutations within the pigment synthesizing pathway and/or proper pigment cell development (Miller et al., 2007). In contrast, lower vertebrates and invertebrates often possess more than one pigment cell type. "
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    ABSTRACT: Retinoic acid (RA) signaling exerts several important functions during vertebrate development. Several cell types derived from neural crest cells (NCC) have been shown to require balanced RA levels for their development. The neural crest is a transient, multipotent embryonic tissue, which also gives rise to melanophores and other pigment cell types. Here, I examined whether RA signaling is involved in NCC-derived melanophore development. My results indicate that enhanced RA levels cause hyperpigmentation in zebrafish larvae by increasing the melanoblast population, most likely by interfering with NCC development. I suggest that RA acts on NCCs, through either enhancing NCC induction, promoting proliferation, or inhibiting NCC apoptosis. It remains to be shown whether RA exerts additional functions within the melanophore lineage or, if the observations are primarily caused by RA´s well known function within NCC development.
    02/2015, Supervisor: Nicola Blum, Gerrit Begemann
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    • "Sticklebacks fall prey to a wide variety of predators, such as aquatic bird, insect, and larger fish species, due to their small size, and thus they have a suite of morphological and behavioral adaptations that defend themselves against predators (Huntingford and Coyle 2007). Sticklebacks exhibit dark coloration particularly in dorsolateral surfaces, which is determined by melanin level and melanophore number, and interestingly both freshwater and marine sticklebacks show striking among-and within-population variations in the amount and pattern of the dark pigmentation (Miller et al. 2007; Greenwood et al. 2011, 2012). These differences are probably associated with ecological differences, particularly in predation pressure, because melanin coloration (brown, gray, and black) against dark background color of river bed or aquatic plants provides crypsis (Price et al. 2008). "
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    ABSTRACT: Predation is a strong selective force that promotes the evolution of anti-predator behaviours and camouflage in prey animals. However, the independent evolution of single traits cannot explain how observed phenotypic variations of these traits are maintained within populations. We studied genetic and phenotypic correlations between anti-predator behaviours (shoaling and risk-taking) and morphology traits (pigmentation and size) in juvenile three-spined sticklebacks by using pedigree-based quantitative genetic analysis to test phenotypic integration (or complex phenotype) as an evolutionary response to predation risk. Individuals with strongly melanised (i.e. camouflaged) phenotype and genotype were less sociable to conspecifics but bolder during foraging under predation risk. Individuals with faster growing phenotype and genotype were bolder, and those with lager eyes were more fearful. These phenotypic integrations were not confounded with correlated plastic responses to predation risk because the phenotypes were measured in naïve fish born in the laboratory but originated from a natural population with predation pressure. Consistent selection for particular combinations of traits under predation pressure or pleiotropic genes might influence the maintenance of the genetic (co)variations and polymorphism in melanin colour, growth trajectory and behaviour patterns.This article is protected by copyright. All rights reserved.
    Evolution 01/2015; 69(3). DOI:10.1111/evo.12600 · 4.61 Impact Factor
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