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: 33.12). 07/2006; 125(7):1387-99. DOI: 10.1016/j.cell.2006.04.043
Source: PubMed

ABSTRACT 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.

1 Follower
  • Source
    • "They could be rooted, however, in both the macroevolutionary traditions of comparative morphology and the omission of embryology from the classic evolutionary synthesis and the emphasis of contemporary evo devo on understanding the development and evolution of body plans and evolutionary novelties. This is not to say that evo devo has completely ignored population thinking and issues of genetic variation: on the contrary, studies of closely related species have provided important insights into morphological evolution (e.g., Stern 1998; Sucena and Stern 2000; Gompel et al. 2005; Jeong et al. 2006, 2008; Rebeiz et al. 2009b; Frankel et al. 2011; Loehlin and Werren 2012). However, an expanded microevo-devo effort can extend this work and provide further examples to test existing hypotheses about phenotypic evolution across a wide range of organisms and traits, especially where suitable closely related species are not available for genetic mapping or reciprocal functional analysis. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The term "micro-evo-devo" refers to the combined study of the genetic and developmental bases of natural variation in populations and the evolutionary forces that have shaped this variation. It thus represents a synthesis of the fields of evolutionary developmental biology and population genetics. As has been pointed out by several others, this synthesis can provide insights into the evolution of organismal form and function that have not been possible within these individual disciplines separately. Despite a number of important successes in micro-evo-devo, however, it appears that evo devo and population genetics remain largely separate spheres of research, limiting their ability to address evolutionary questions. This also risks pushing contemporary evo devo to the fringes of evolutionary biology because it does not describe the causative molecular changes underlying evolution or the evolutionary forces involved. Here we reemphasize the theoretical and practical importance of micro-evo-devo as a strategy for understanding phenotypic evolution, review the key recent insights that it has provided, and present a perspective on both the potential and the remaining challenges of this exciting interdisciplinary field.
    Genetics 11/2013; 195(3):625-34. DOI:10.1534/genetics.113.156463 · 4.87 Impact Factor
  • Source
    • "An earlier report showed that the Ubx gene regulated pigmentation in the hindwings of the butterfly Precis coenia (Weatherbee et al., 1999). In addition, an intriguing case in which Hox protein abdominal-B (abd-B) directly activated expression of the yellow pigmentation gene in the D. melanogaster, demonstrated the relevance between Hox genes and pigmentation genes (Jeong et al., 2006). Consideration of either phenomenon should be focused on the relation between pigmentation and other Hox genes. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Homeotic genes, which are associated closely with body patterning of various species, specify segment identity. The Wedge eye-spot (Wes) is a new homeotic mutant located on the sixth linkage group. Homozygous Wes/Wes embryos are lethal and display a pair of antenna-like appendages under the mouthparts as well as fused thoracic segments. These mutants also exhibit a narrower eye-spot at the larval stage compared with the wild type. By positional cloning, we identified the candidate gene of the Wes locus, Bombyx mori Antennapedia (BmAntp). Two BmAntp transcripts were identified in the homozygote of the Wes mutant, including a normal form and an abnormal form with a 1570-bp insertion. Our data showed that the insertion element was a long interspersed nuclear element (LINE)-like transposon that destroyed the original open reading frame of BmAntp. Quantitative RT-PCR analysis showed that the expression levels of normal BmAntp transcripts were increased markedly in the Wes heterozygous larvae compared with the wild type. Furthermore, we performed RNAi of BmAntp and observed fused thoracic segments and defective thoracic legs in the developing embryos. Our results indicated that BmAntp is responsible for the Wes mutant and has an important role in determining the proper development of the thoracic segments. Our identification of a homeotic mutation in the silkworm is an important contribution to our understanding of the regulation of Hox genes at different levels of expression.Heredity advance online publication, 8 May 2013; doi:10.1038/hdy.2013.36.
    Heredity 05/2013; DOI:10.1038/hdy.2013.36 · 3.80 Impact Factor
  • Source
    • "Repression of y by female-specific expression of Bab blocks posterior abdominal pigmentation . Evolution of CREs controlling expression of bab and y has repeatedly led to novel and convergent abdominal pigment pattern within the Drosophilidae family (Gompel and Carroll, 2003; Jeong et al., 2006; Williams et al., 2008). Similar cooperative genetic interactions controlling the development and evolution of male-specific tarsal sex combs have been characterized for Dsx and the Hox protein Sex-combs reduced (Scr; Barmina et al., 2005; Barmina and Kopp, 2007; Tanaka et al., 2011). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Hox transcription factors are deeply conserved proteins that guide development through regulation of diverse target genes. Furthermore, alteration in Hox target cis-regulation has been proposed as a major mechanism of animal morphological evolution. Crucial to understanding how homeotic genes sculpt the developing body and contribute to the evolution of form is identification and characterization of regulatory targets. Because target specificity is achieved through physical or genetic interactions with cofactors or co-regulators, characterizing interactions between homeotic genes and regulatory partners is also critical. In Drosophila melanogaster, sexually dimorphic abdominal morphology results from sex-specific gene regulation mediated by the Hox protein Abdominal-B (Abd-B) and products of the sex-determination gene doublesex (dsx). Together these transcription factors regulate numerous sex-specific characters, including pigmentation, cuticle morphology, and abdominal segment number. We show Dsx expression in the developing D. melanogaster pupal abdomen is spatiotemporally dynamic, correlating with segments that undergo sexually dimorphic morphogenesis. Furthermore, our genetic analyses show Dsx expression is Abd-B dependent. Doublesex and Abd-B are not only requisite co-regulators of sexually dimorphic abdominal morphology. We propose that dsx is itself a transcriptional target of Abd-B. These data present a testable hypothesis about the evolution of sexually dimorphic segment number in Diptera.
    Developmental Dynamics 06/2012; 241(6):1076-90. DOI:10.1002/dvdy.23791 · 2.67 Impact Factor
Show more


Available from