Adaptation to long sperm in Drosophila: correlated development of the sperm roller and sperm packaging

Sperm are generally small and produced in huge numbers, but some species combine exaggerated sperm length with extremely limited numbers of sperm, an evolutionary trend that deviates from the theory of anisogamy. Sperm gigantism has arisen recurrently in various species, but insects exhibit the longest sperm, with some species of the Drosophilidae family producing sperm up to 6 cm in length. The anatomical, cytological, and physiological requirements for males to cope with these giant sperm were hitherto poorly understood. In this paper, we investigate the internal morphology of the male reproductive tract, and highlight specific features that may be linked to this increase in sperm size. We focus on species in the repleta group, within which sperm length varies by a factor of 35. An associated development of the sperm roller, a special twisting device inserted between the testis and the seminal vesicle, is demonstrated. Its length and the number of coils involved increase with sperm size, and it allows individual sperm to swell and roll into a spermatic pellet before reaching the seminal vesicle. This process occurs independently of and in addition to the sperm bundle coiling that takes place at the base of the testis. It is suggested that the emergence and development of the sperm roller may be a male adaptation to sperm gigantism.