Sex-specific differentiation of a male-specific abdominal muscle, the Muscle of Lawrence, is abnormal in hydroxyurea-treated and in fruitless male flies

Abstract

A prominent sex-specific abdominal muscle in male Drosophila is the Muscle of Lawrence (MOL), which is induced by male-specific innervation. We have examined MOL development in wild-type males, in males fed hydroxyurea to ablate the muscle precursors and in fruitless mutants, in which the MOL muscle develops aberrantly. One striking feature of MOLs in wild-type males was the presence of additional muscle nuclei compared with neighboring muscles or MOL-homologues in females. We tested whether muscle length and the sex-specific expression of a reporter gene depended critically on the number of nuclei present within a MOL fiber. MOL fibers developing from a reduced myoblast pool in hydroxyurea-affected hemisegments were recognizable by their attachment points and still contained more nuclei than did neighboring medial fibers, suggesting that these MOL fibers were able to actively recruit myoblasts nearly as well as wild-type MOLs. However, many of the hydroxyurea-affected MOL fibers were incapable of the normal male-specific expression of a muscle-specific reporter gene. We suggest that early events in MOL development, such as finding the correct muscle attachment points, are relatively insensitive to the number of MOL nuclei compared with later events, such as the sex-specific expression of a reporter gene. In fruitless mutant males, MOL-position fibers are smaller and had substantially fewer nuclei compared to wild-type MOLs. Since the number and distribution of muscle precursors was the same in fruitless mutant and wild-type animals, we propose that one fru+ function is to direct the male-specific recruitment of myoblasts into MOL-myotubes. However, fruitless+ must have more than one role in MOL fiber development, since simple reduction in the number of muscle nuclei, as demonstrated by the hydroxyurea ablations, is insufficient to account for all of the MOL muscle phenotypes in fruitless mutant males.