Regulation of Body Pigmentation by the Abdominal-B Hox Protein and Its Gain and Loss in Drosophila Evolution

Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, 1525 Linden Drive, Madison, WI 53706, USA.
Cell (Impact Factor: 32.24). 07/2006; 125(7):1387-99. DOI: 10.1016/j.cell.2006.04.043
Source: PubMed


Hox genes have been implicated in the evolution of many animal body patterns, but the molecular events underlying trait modification have not been elucidated. Pigmentation of the posterior male abdomen is a recently acquired trait in the Drosophila melanogaster lineage. Here, we show that the Abdominal-B (ABD-B) Hox protein directly activates expression of the yellow pigmentation gene in posterior segments. ABD-B regulation of pigmentation evolved through the gain of ABD-B binding sites in a specific cis-regulatory element of the yellow gene of a common ancestor of sexually dimorphic species. Within the melanogaster species group, male-specific pigmentation has subsequently been lost by at least three different mechanisms, including the mutational inactivation of a key ABD-B binding site in one lineage. These results demonstrate how Hox regulation of traits and target genes is gained and lost at the species level and have general implications for the evolution of body form at higher taxonomic levels.

    • "In the 6 ancestral range in Africa, geographic variation is most strongly associated with levels 7 of UV-radiation, consistent with higher UV tolerance of darkly pigmented flies 8 compared to light ones (Bastide et al. 2014). 9 There have been several previous studies of pigmentation variation in 10 Drosophila, describing the genetic basis of variation in abdominal pigmentation 11 between species and between sexes (Llopart et al. 2002; Wittkopp et al. 2003; 12 Gompel et al. 2005; Jeong et al. 2006, 2008; Williams et al. 2008; Rogers et al. 2013; 13 Rogers et al. 2014; Salomone et al. 2013), and on variation in thoracic and abdominal 14 pigmentation within species (Robertson et al. 1977; Pool and Aquadro 2007; 15 Takahashi et al. 2007; Bickel et al. 2011; Takahashi and Takano-Shimizu 2011; 16 Bastide et al. 2013; Rogers et al. 2014; Dembeck et al. 2015; Wittkopp et al. 2010; 17 Cooley et al. 2012). The latter studies are the most relevant here. "
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    ABSTRACT: The degree of concordance between populations in the genetic architecture of a given trait is an important issue in medical and evolutionary genetics. Here, we address this problem, using a replicated pooled genome wide association approach (Pool-GWAS) to compare the genetic basis of variation in abdominal pigmentation in female European and South African Drosophila melanogaster. We find that, in both the European and the South African flies, variants near the tan and bric-à-brac 1 (bab1) genes are most strongly associated with pigmentation. However, the relative contribution of these loci differs: in the European populations, tan outranks bab1, while the converse is true for the South African flies. Using simulations, we show that this result can be explained parsimoniously, without invoking different causal variants between the populations, by a combination of frequency differences between the two populations and dominance for the causal alleles at the bab1 locus. Our results demonstrate the power of cost-effective, replicated Pool-GWAS to shed light on differences in the genetic architecture of a given trait between populations.
    No preview · Article · Dec 2015 · Genetics
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    • "Evolutionary modification of this developmental process in different animal lineages has given rise to the vast diversity of body form and function observed across the Metazoa today. Many evolutionary changes to genes have been documented including gene duplications (Brooke et al. 1998; Putnam et al. 2008), coding sequence alterations (Fondon and Garner 2004), and modifications to gene expression (Jeong et al. 2006). Although much focus has been on the evolution of cis-regulatory elements that affect gene expression (Putnam et al. 2008; Chan et al. 2010), there are also trans-acting factors that should not be overlooked. "
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    ABSTRACT: MicroRNAs (miRNAs) are involved in post-transcriptional regulation of gene expression l regulation of gene expressionvelopment to reory genese likely false positives. too approximate.rgence times that I cited init. Since several miRNAs are known to affect the stability or translation of developmental regulatory genes, the origin of novel miRNAs may have contributed to the evolution of developmental processes and morphology. Lepidoptera (butterflies and moths) is a species-rich clade with a well-established phylogeny and abundant genomic resources, thereby representing an ideal system in which to study miRNA evolution. We sequenced small RNA libraries from developmental stages of two divergent lepidopterans, Cameraria ohridella (Horse chestnut Leafminer) and Pararge aegeria (Speckled Wood butterfly), discovering 90 and 81 conserved miRNAs respectively, and many species-specific miRNA sequences. Mapping miRNAs onto the lepidopteran phylogeny reveals rapid miRNA turnover and an episode of miRNA fixation early in lepidopteran evolution, implying that miRNA acquisition accompanied the early radiation of the Lepidoptera. One lepidopteran-specific miRNA gene, miR-2768, is located within an intron of the homeobox gene invected, involved in insect segmental and wing patterning. We identified cubitus interruptus (ci) as a likely direct target of miR-2768, and validated this suppression using a luciferase assay system. We propose a model by which miR-2768 modulates expression of ci in the segmentation pathway and in patterning of lepidopteran wing primordia. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Full-text · Article · Jan 2015 · Molecular Biology and Evolution
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    • "In the posterior abdominal segments of females, Abd-B and a female-isoform of Dsx directly activate bab expression, and then Bab represses yellow expression [39], [41]. In those of males, Abd-B and a male-isoform of Dsx repress bab expression, resulting in the male- and segment-specific patterns of yellow expression [39], [41]. Suppressive regulations of bab with sexually dimorphic pigmentation would have independently occurred several times, at least within the genus Drosophila [42], [43]. "
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    ABSTRACT: Most hymenopteran species exhibit conspicuous sexual dimorphism due to ecological differences between the sexes. As hymenopteran genomes, under the haplodiploid genetic system, exhibit quantitative differences between sexes while remaining qualitatively identical, sexual phenotypes are assumed to be expressed through sex-specific gene usage. In the present study, the molecular basis for expression of sexual dimorphism in a queenless ant, Diacamma sp., which exhibits a distinct color dimorphism, was examined. Worker females of the species appear bluish-black, while winged males exhibit a yellowish-brown body color. Initially, observations of the pigmentation processes during pupal development revealed that black pigmentation was present in female pupae but not in males, suggesting that sex-specific melanin synthesis was responsible for the observed color dimorphism. Therefore, five orthologs of the genes involved in the insect melanin synthesis (yellow, ebony, tan, pale and dopa decarboxylase) were subcloned and their spatiotemporal expression patterns were examined using real-time quantitative RT-PCR. Of the genes examined, yellow, which plays a role in black melanin synthesis in insects, was expressed at higher levels in females than in males throughout the entire body during the pupal stage. RNA interference of yellow was then carried out in order to determine the gene function, and produced females with a more yellowish, brighter body color similar to that of males. It was concluded that transcriptional regulation of yellow was responsible for the sexual color dimorphism observed in this species.
    Full-text · Article · Mar 2014 · PLoS ONE
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