Modular tissue-specific regulation of doublesex underpins sexually dimorphic development in Drosophila

Abstract

The ability of a single genome to produce distinct and often dramatically different male and female forms is one of the wonders of animal development. In Drosophila melanogaster, most sexually dimorphic traits are controlled by sex-specific isoforms of the doublesex (dsx) transcription factor, and dsx expression is mostly limited to cells that give rise to sexually dimorphic traits. However, it is unknown how this mosaic of sexually dimorphic and monomorphic organs arises. Here, we characterize the cis-regulatory sequences that control dsx expression in the foreleg, which contains multiple types of sex-specific sensory organs. We find that separate modular enhancers are responsible for dsx expression in each sexually dimorphic organ. Expression of dsx in the sex comb is co-regulated by two enhancers with distinct spatial and temporal specificities that are separated by a genitalia-specific enhancer. The sex combspecific enhancer from D. willistoni, a species that primitively lacks sex combs, is not active in the foreleg. Thus, the mosaic of sexually dimorphic and monomorphic organs depends on modular regulation of dsx transcription by dedicated cell type-specific enhancers.

The yellow gene influences Drosophila male mating success through sex comb melanization

“…42D04-GAL4 also drives expression in male and female larval CNS and genital discs, with expression in the genital tissues persisting into the adult stage only in females (Figure 3—figure supplement 1C–G). Finally, we observed 42D04-GAL4 expression at the base of the sex combs (also observed by Robinett et al, 2010 and Rice et al, 2019), which are modified bristles used during mating (Cook, 1975; Ng and Kopp, 2008; Hurtado-Gonzales et al, 2015) that are present only on the first tarsal segment of adult male forelegs (Figure 3C–F). Yellow protein is expressed in sex combs (Hinaux et al, 2018, Figure 3G,H), where it is presumably required for synthesis of black dopamine melanin in the sex comb ‘teeth’.…”

An Atlas of Transcription Factors Expressed in Male Pupal Terminalia ofDrosophila melanogaster

“…We found that esg is expressed at the base of both pairs of postgonites, while fd96Cb was expressed throughout both pairs of postgonites. We also found that retn (Figure 6F) and dsx (see images at https://flyterminalia.pitt.edu/) are expressed in the ventral postgonites, but not the dorsal pair, and we note that dsx has a known enhancer that drives expression in this region (Rice et al 2019a). Taken together, we identified genes that are expressed in distinct phallic structures, as well as within subcompartments of individual structures.…”

“…In this study, we found several genes that are expressed in lateral gonocoxite ( esg , inv , en ), and postgonites ( esg , fd96Cb , crp , mod , retn and dsx ), both of which exhibit morphological changes between species. Furthermore, a ventral postgonite enhancer was recently identified for the gene doublesex (Rice et al 2019a ) which may serve as a useful driver to manipulate this structure in future studies. Other enhancers that drive expression in the larval genital disc may persist in the pupal terminalia and prove useful as drivers to target other structures (Jory et al 2012).…”

Doublesexmediates species-, sex-, environment- and trait-specific exaggeration of size and shape

“…Diptera [50], Lepidoptera [51,52], Hymenoptera [41] and Coleoptera [14,16]) and commonly exhibits a high degree of tissue specificity (e.g. [53]), dsx is likely to contribute to the resolution of trait-specific sexual conflict in a broad range of arthropods.…”