Sex-specific repression of dachshund is required for Drosophila sex comb development

Abstract

The origin of new morphological structures requires the establishment of new genetic regulatory circuits to control their development, from initial specification to terminal differentiation. The upstream regulatory genes are usually the first to be identified, while the mechanisms that translate novel regulatory information into phenotypic diversity often remain obscure. In particular, elaborate sex-specific structures that have evolved in many animal lineages are inevitably controlled by sex-determining genes, but the genetic basis of sexually dimorphic cell differentiation is rarely understood. In this report, we examine the role of dachshund (dac), a gene with a deeply conserved function in sensory organ and appendage development, in the sex comb, a recently evolved male-specific structure found in some Drosophila species. We show that dac acts during metamorphosis to restrict sex comb development to the appropriate leg region. Localized repression of dac by the sex determination pathway is necessary for male-specific morphogenesis of sex comb bristles. This pupal function of dac is separate from its earlier role in leg patterning, and Dac at this stage is not dependent on the pupal expression of Distalless (Dll), the main regulator of dac during the larval period. Dll acts in the epithelial cells surrounding the sex comb during pupal development to promote sex comb rotation, a complex cellular process driven by coordinated cell rearrangement. Our results show that genes with well-conserved developmental functions can be re-used at later stages in development to regulate more recently evolved traits. This mode of gene co-option may be an important driver of evolutionary innovations.

Exaggerated Trait Growth in Insects

“…Specifically, dsx controls sex-specific trait growth by binding cis-regulatory regions of downstream target genes (114,162,192). Both general and tissue-specific expression modifications of dsx can contribute to sexual dimorphism in trait size (90,109,153,168) by controlling downstream patterning genes responsible for trait development, as observed for primary sexual traits such as genital structures and gonads (5,24,87,153) and secondary traits such as the male-specific sex combs of some Drosophila flies (6,168).…”

The retinal determination genedachshundrestricts cell proliferation by limiting the activity of the Homothorax-Yorkie complex

“…6), in the wing blade, ectopic Dac might limit ban expression by restricting the activity of the Yki-Mad or Yki-Sd complexes on additional enhancers. In addition, Dac appears to regulate the expression of distinct sets of patterning genes depending of the cellular context, as dac is also required for establishing the segmental pattern of Notch ligand and fringe expression in the leg imaginal disc, for sensory organ, genitalia and sex comb development and for proper neuronal differentiation (Atallah et al, 2014;Keisman and Baker, 2001;Martini et al, 2000;Miguel-Aliaga et al, 2004;Okamoto et al, 2012;Rauskolb, 2001). …”

Genetic dissection of intraspecific variation in a male-specific sexual trait in Drosophila melanogaster

“…Several genes are known to affect the specification and development of the sex comb, such as Scr (Lewis et al , 1980a, b; Barmina and Kopp, 2007; Tanaka et al , 2011), dac (Atallah et al , 2014), the sex determination pathway genes dsx and transformer 2 , tra2 (Baker and Ridge, 1980; Tanaka et al , 2011) and a series of genes named based on their effect on the sex comb ( Additional sex combs , extra sex combs , multi sex combs , Posterior sex combs , Sex comb on midleg , Sex combs extra and super sex combs ). Although some of these genes, such as dsx and Scr (Graze et al , 2007), have been implicated within QTL intervals identified in previous mapping studies, none of them are present within the three QTLs we map in the DSPR (Supplementary File S7).…”

“…None of the three QTLs we map implicate dac , dsx , Scr or tra2 (Supplementary File S7), the four genes that have been shown to be involved in the specification and development of the sex comb (Baker and Ridge, 1980; Lewis et al , 1980a, b; Barmina and Kopp, 2007; Tanaka et al , 2011; Atallah et al , 2014). Although not formally significant at a 5% permutation-derived threshold (Churchill and Doerge, 1994), we observed three additional peaks in the LOD (logarithm (base 10) of odds) score profile that are close to genome-wide significance (X, 0.5 cM; 2L, 54.0 cM; and 2R, 87.5 cM; Figure 2 and Supplementary File S3).…”

“…Scr serves to activate doublesex ( dsx ) in the tarsal region during the late larval stage, and dsx expression subsequently initiates sex-specific development of the comb, and defines its morphology (Tanaka et al , 2011). The role of dsx in the morphogenesis of the sex comb appears to be at least partly carried out through a repression of dachshund ( dac ) as Dac is absent from the sex comb during pupal development (Atallah et al , 2009, 2014,). An unanswered question is whether these high-level developmental regulatory genes that are responsible for development of the sex comb also segregate for allelic variation that confers intraspecific variation in sex comb morphology.…”