Multinucleated smooth muscles and mononucleated as well as multinucleated striated muscles develop during establishment of the male reproductive organs of Drosophila melanogaster

The adult musculature in D. melanogaster forms during metamorphosis. Much is known about the flight and leg musculature, but not about the muscles surrounding the male reproductive tract. The inner genitalia of males consist of the testes, which emerge from the gonads; the remaining genital organs, i.e., paragonia (or accessory glands), ejaculatory duct, sperm pump, and seminal vesicles, develop out of the genital imaginal disc. We analyzed the myoblasts forming the muscle layers of these organs. In myoblasts derived from the genital imaginal disc, the regulatory region of the transcription factor DMef2 is active. DMef2 is also needed for specification and differentiation of embryonic and adult myoblasts. We could discriminate three different muscle types: (i) multinucleated muscles that resemble vertebrate smooth muscles surround the testes, (ii) multinucleated muscles that resemble striated muscles comprises seminal vesicles and the sperm pump, and (iii) mononucleated striated musculature encloses the paragonia and ejaculatory duct. Members of the immunoglobulin superfamily involved in embryonic myogenesis, Dumbfounded (Duf) and Sticks and Stones (Sns), were also expressed in the genital imaginal disc, in the muscle sheath of the testes during muscle differentiation and in the secretory secondary cells, which are part of the binucleated epithelia enclosing the paragonia.

► We found multinucleated, striated and smooth muscles around the adult male reproductive tract.
► For the first time multinucleated, smooth muscle-like cells are reported in adult Drosophila.
► We analyzed the morphology of the male genital imaginal disc during metamorphosis.
► Sns and Duf are active in myoblasts on the imaginal disc, suggesting fusion events on pupal testes.
► Multinucleated, nascent myofibers arrive at the distal part of the testes and migrate to proximal.