The Developmental Role of Agouti in Color Pattern Evolution

Manceau, Marie; Domingues, Vera; Mallarino, Ricardo; Hoekstra, Hopi E.

doi:10.1126/science.1200684

Cited by 207 publications

(201 citation statements)

References 26 publications

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“…Indeed, this is what we observed for the endocytosis complex adaptations, whose pleiotropic effects on morphology have apparently been compensated by other loci. Another point of contrast is that nearly all previous studies of cis-regulatory adaptation have focused on single genes (with a few exceptions [Fraser 2011]) (Shapiro et al 2004;Colosimo et al 2005;Gompel et al 2005;Miller et al 2007;Prud'homme et al 2007;Wray 2007;Rebeiz et al 2009, Manceau et al 2011. Our results highlight a previously unknown mode of evolution: polygenic cis-regulatory adaptation acting at the level of a physically interacting module.…”

Section: Discussioncontrasting

confidence: 54%

“…The first identifies single genes whose expression affects an adaptive trait, often via QTL mapping of the trait followed by detailed investigation of candidate genes. This approach has led to several fascinating examples of gene expression adaptations (Shapiro et al 2004;Colosimo et al 2005;Gompel et al 2005;Miller et al 2007;Prud'homme et al 2007;Wray 2007;Rebeiz et al 2009;Manceau et al 2011). However, the amount of effort required-as well as the need for previously characterized candidate genes within each QTL region-has limited its general applicability.…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

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Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity

et al. 2012

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The acquisition of new genes, via horizontal transfer or gene duplication/diversification, has been the dominant mechanism thus far implicated in the evolution of microbial pathogenicity. In contrast, the role of many other modes of evolution-such as changes in gene expression regulation-remains unknown. A transition to a pathogenic lifestyle has recently taken place in some lineages of the budding yeast Saccharomyces cerevisiae. Here we identify a module of physically interacting proteins involved in endocytosis that has experienced selective sweeps for multiple cis-regulatory mutations that down-regulate gene expression levels in a pathogenic yeast. To test if these adaptations affect virulence, we created a panel of single-allele knockout strains whose hemizygous state mimics the genes' adaptive down-regulations, and measured their virulence in a mammalian host. Despite having no growth advantage in standard laboratory conditions, nearly all of the strains were more virulent than their wild-type progenitor, suggesting that these adaptations likely played a role in the evolution of pathogenicity. Furthermore, genetic variants at these loci were associated with clinical origin across 88 diverse yeast strains, suggesting the adaptations may have contributed to the virulence of a wide range of clinical isolates. We also detected pleiotropic effects of these adaptations on a wide range of morphological traits, which appear to have been mitigated by compensatory mutations at other loci. These results suggest that cis-regulatory adaptation can occur at the level of physically interacting modules and that one such polygenic adaptation led to increased virulence during the evolution of a pathogenic yeast.

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Section: Discussioncontrasting

confidence: 54%

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity

et al. 2012

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“…Deer mice display extensive pigment variation matching the color of their environment (Manceau et al 2010). Fine mapping of this variation revealed that not only the Agouti locus is the major driver of pigment variation (Manceau et al 2011) but also this genetic region decomposes itself into multiple noncoding sub-loci, each tightly associated with parts of the total phenotype (Linnen et al 2013). Various regulatory elements are involved in directing the expression of three alternative isoforms into different body regions (Mallarino et al 2016).…”

Section: Cis-regulatory Evolution Drives Regional Specific Color Shiftsmentioning

confidence: 99%

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Martin

Courtier‐Orgogozo

2017

Diversity and Evolution of Butterfly Wing Patterns

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What types of genetic changes underlie evolution? Secreted signaling molecules (syn. ligands) can induce cells to switch states and thus largely contribute to the emergence of complex forms in multicellular organisms. It has been proposed that morphological evolution should preferentially involve changes in developmental toolkit genes such as signaling pathway components or transcription factors. However, this hypothesis has never been formally confronted to the bulk of accumulated experimental evidence. Here we examine the importance of ligandcoding genes for morphological evolution in animals. We use Gephebase (http:// www.gephebase.org), a database of genotype-phenotype relationships for evolutionary changes, and survey the genetic studies that mapped signaling genes as causative loci of morphological variation. To date, 19 signaling genes represent 20% of the cases where an animal morphological change has been mapped to a gene (80/391). This includes the signaling gene Agouti, which harbors multiple cis-regulatory alleles linked to color variation in vertebrates, contrasting with the effects of coding variation in its target, the melanocortin receptor MC1R. In sticklebacks, genetic mapping approaches have identified 4 signaling genes out of 14 loci associated with lake adaptations. Finally, in butterflies, a total of 18 allelic variants of the WntA Wnt-family ligand cause color pattern adaptations related to wing mimicry, both within and between species. We discuss possible hypotheses explaining these cases of natural replication (genetic parallelism) and conclude that signaling ligand loci are an important source of sequence variation underlying morphological change in nature.

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“…This circumvention of pleiotropy by changes in gene regulation, recently dubbed the Stern-Carroll Rule (3), has been borne out in both animals and plants (e.g., refs. [4][5][6][7][8][9][10]. In each case, transcriptional enhancers appear to have been the target of selection.…”

mentioning

confidence: 99%

Independent recruitments of a translational regulator in the evolution of self-fertile nematodes

Beadell

Liu²,

Johnson³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Pleiotropic developmental regulators have been repeatedly linked to the evolution of anatomical novelties. Known mechanisms include cis-regulatory DNA changes that alter regulator transcription patterns or modify target-gene linkages. Here, we examine the role of another form of regulation, translational control, in the repeated evolution of self-fertile hermaphroditism in Caenorhabditis nematodes. Caenorhabditis elegans hermaphrodites initiate spermatogenesis in an otherwise female body through translational repression of the gene tra-2. This repression is mediated by GLD-1, an RNA-binding protein also required for oocyte meiosis and differentiation. By contrast, we show that in the convergently hermaphroditic Caenorhabditis briggsae, GLD-1 acts to promote oogenesis. The opposite functions of gld-1 in these species are not gene-intrinsic, but instead result from the unique contexts for its action that evolved in each. In C. elegans, GLD-1 became essential for promoting XX spermatogenesis via changes in the tra-2 mRNA and evolution of the species-specific protein FOG-2. C. briggsae GLD-1 became an essential repressor of sperm-promoting genes, including Cbr-puf-8, and did not evolve a strong association with tra-2. Despite its variable roles in sex determination, the function of gld-1 in female meiotic progression is ancient and conserved. This conserved role may explain why gld-1 is repeatedly recruited to regulate hermaphroditism. We conclude that, as with transcription factors, spatially localized translational regulators play important roles in the evolution of anatomical novelties.germ cells | translation | breeding systems | mutant

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The Developmental Role of Agouti in Color Pattern Evolution

Abstract: A regulatory mutation affecting expression of the Agouti gene shows color-specific selection in beach mice.

Cited by 207 publications

References 26 publications

Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity

Polygenic cis-regulatory adaptation in the evolution of yeast pathogenicity

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

Independent recruitments of a translational regulator in the evolution of self-fertile nematodes

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