Rewired gene interactions during development of serially homologous appendages in male and female Drosophila

Abstract

Drosophila ventral appendages are considered to be serially homologous derived from a ventral appendage ground state and shaped by different Hox inputs. In the legs and antennae a combination of the transcription factors C15, LIM1 homeobox 1 (Lim1), and Al (Aristaless) is required for the development of the tarsal claws and aristae, respectively. However, the roles of these factors in genital development have remained unexplored. Here, we investigated the expression and function of C15, Lim1, and Al in the development of male and female terminalia (genitalia and analia). We found that C15 plays distinct roles in males and females, repressing male clasper bristle formation while promoting bristle development in the female epiproct. Unlike in the antennal and leg discs, C15, Lim1, and Al are not all simultaneously co-expressed in any anal or genital structures in either sex, indicating that the interactions among these factors have diverged across these appendages. Nevertheless, we inferred regulatory interactions between C15 and other factors, reflecting similarities between leg and male clasper development. Finally, we identified a male-specific C15 enhancer that is active in male claspers but not in the female epiproct, legs or antennae. This C15 enhancer modularity may underpin tissue- and sex-specific regulatory logic.