Sexually dimorphic regulation of the Wingless morphogen controls sex-specific segment number in Drosophila

Abstract

Sexual dimorphism is widespread throughout the metazoa and plays important roles in mate recognition and preference, sexbased niche partitioning, and sex-specific coadaptation. One notable example of sex-specific differences in insect body morphology is presented by the higher diptera, such as Drosophila, in which males develop fewer abdominal segments than females. Because diversity in segment number is a distinguishing feature of major arthropod clades, it is of fundamental interest to understand how different numbers of segments can be generated within the same species. Here we show that sex-specific and segment-specific regulation of the Wingless (Wg) morphogen underlies the development of sexually dimorphic adult segment number in Drosophila. Wg expression is repressed in the developing terminal male abdominal segment by the combination of the Hox protein Abdominal-B (Abd-B) and the sex-determination regulator Doublesex (Dsx). The subsequent loss of the terminal male abdominal segment during pupation occurs through a combination of developmental processes including segment compartmental transformation, apoptosis, and suppression of cell proliferation. Furthermore, we show that ectopic expression of Wg is sufficient to rescue this loss. We propose that dimorphic Wg regulation, in concert with monomorphic segment-specific programmed cell death, are the principal mechanisms of sculpting the sexually dimorphic abdomen of Drosophila.morphogenesis | segmentation | homeotic | epithelia B rachycera, higher diptera that include drosophilidae, exhibit an evolutionary trend toward reduced abdominal size that contributes to swift, maneuverable flight (1). Such reduction is especially pronounced within the infraorder Muscomorpha. Within this group of flies, abdominal reduction is sexually dimorphic such that adult males have fewer segments than females. Lower diptera, which includes mosquitoes and midges, retain ancestral morphology with respect to segment number; both adult males and females generate eight abdominal segments. In Muscomorpha the most posterior adult abdominal segments (all or a subset of segments A5-A8) are modified in females, usually as a telescoping ovipositor, whereas corresponding segments are absent in males (2). In all diptera, segment number is monomorphic during embryogenesis and larval development, reflecting the basal insect body plan of three head, three thoracic, and 11 abdominal segments. For most diptera, only embryonic abdominal segments 1-8 generate adult abdominal tissue (only segments 1-7 in the drosophilidae). The more posterior embryonic segments contribute to the adult genitalia. During pupation, sex-specific developmental programs are deployed that sculpt sexually dimorphic segment morphology and number.The posterior abdomen of Drosophila melanogaster serves as an excellent model to study the development of these sex-specific morphologies. Posterior abdominal segment identity, morphology, and number in both sexes is regulated by the Hox protein Abdominal-B (Abd-B) (3, 4). Abd-B ex...

Drosophila Hox and Sex-Determination Genes Control Segment Elimination through EGFR and extramacrochetae Activity

“…In Abd-B mutants there is ectopic wg in the male A7 [15], and this is important for the formation of the segment since the Abd-B mutant phenotype is partially rescued by diminishing wg activity (Figure S4B, compare with Figure 1H). To see if emc works in the A7 by regulating wg we looked to wg expression when Emc function is compromised.…”

“…If we elevate this activity in the male A7 we observe an increase the number of histoblasts, that many of these cells remain at the surface at the time of extrusion and that a small A7 forms in the adult. It was also previously reported that a small A7 is observed in the male adult when expressing vein , an EGFR ligand [15]. It is possible that the high number of histoblasts obtained when over-expressing elements of the EGFR pathway makes many of them unable to be extruded by a “titration” effect, that is, there may be “too many” histoblasts for the invagination mechanism to extrude them at the correct time.…”

Sex- and Tissue-Specific Functions of Drosophila Doublesex Transcription Factor Target Genes

“…These cell types derive from all primary germ layers and have diverse roles in metabolism, gametogenesis, morphology, and behavior. While the transcriptional inputs to dsx expression are not fully understood, Drosophila HOX and other patterning genes regulate dsx in at least some tissues (Foronda et al, 2012; Tanaka et al, 2011; Wang et al, 2011; Wang and Yoder, 2012; Yoder, 2012). …”

Lepidopteran Sex Determination: A Cascade of Surprises

“…These protein isoforms share a common Doublesex-Mab3 domain but contain different dimerization domains [Erdman and Burtis, 1993;Erdman et al, 1996]. As a result, female-and male-specific DSX proteins regulate a number of cytodifferentiation genes in an antagonistic manner [Burtis et al, 1991;Coschigano and Wensink, 1993;Shirangi et al, 2009;Chatterjee et al, 2011;Wang et al, 2011].…”