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.
Sperm competition is expected to be a driving force in sexual selection. In internally fertilized organisms, it occurs when ejaculates from more than one male are present simultaneously within the female's reproductive tract. It has been suggested that greater sperm size may improve the competitive ability of sperm, but studies provide contradictory results depending on the species. More recently, the role of females in the evolution of sperm morphology has been pointed out. We investigate here the male and female effects that influence sperm precedence in the giant sperm species, Drosophila bifurca Patterson & Wheeler. Females were mated with two successive males, and the paternity outcomes for both males were analyzed after determining sperm transfer and storage. We found very high values of last male sperm precedence, suggesting a strong interaction between rival sperm. However, the data also indicate high frequencies of removal of the sperm of the first male from the female reproductive tract prior to any interaction with the second male. This implies that successful paternity depends mainly on successful sperm storage. Knowing what happens to the sperm within females appears to be a prerequisite for disentangling post-copulatory sexual interactions between males and females.
Unlike mammals, where the males produce huge quantities of tiny spermatozoa, insects, and Drosophila in particular, exhibit a wide range of reproductive strategies. Sperm gigantism in Drosophila deviates from the rules that normally govern anisogamy, i.e. differences in the size and quantity of male and female gametes. Sperm gigantism has driven anatomical, physiological and cytological adaptations that affect the correlated evolution of the male and female reproductive systems, and has led to the evolution of a new structure, the roller, located between the testis and the seminal vesicle, and to sperm coiling to form pellets. The diversification of sperm strategy is investigated in the light of sexual selection processes that occur in the female genital tract after copulation. These processes, which bias paternity, result from interactions either between spermatozoa from different males, or between the spermatozoa and the environment within the female reproductive tract. In Drosophila, increased sperm size does not confer any reproductive advantage on the male. The evolution of sperm gigantism does not seem to be attributable to competition between spermatozoa from different males, as has been shown to occur in some vertebrate species. Alternative mechanisms, such as interactions between spermatozoa and the female reproductive system, are therefore currently viewed as being more likely explanations. In particular, the impact of sperm size on female reproductive physiology is being investigated to find out whether having large spermatozoa increases the likelihood of male reproductive success. Correlated adaptations of the spermatozoa and female storage organs also seem to be a major factor in determining sperm success, and their role in male-female conflicts is discussed briefly.
In Drosophila melanogaster, the hobo transposable element is responsible for a hybrid dysgenesis syndrome. It appears in the germline of progenies from crosses between females devoid of hobo elements (E) and males bearing active hobo elements (H). In the HE system, permissivity is the ability of females to permit hobo activity in their progeny when they have been crossed with H males. Permissivity displays both intra- and inter-strain variability and decreases with the age of the females. Such characteristics are reminiscent of those for the reactivity in the IR system. The reactivity is the ability of R females (devoid of I factors) to permit activity of the I LINE retrotransposon in the F1 females resulting from crosses with I males (bearing I factors). Here we investigated permissivity properties in the HE system related to reactivity in the IR system. Previously it had been shown that reactivity increases with the number of Su(var)3-9 genes, which increases chromatin compaction near heterochromatin. Using the same lines, we show that permissivity increases with the number of Su(var)3-9 genes. To investigate the impact of chromatin compaction on permissivity we have tested the polymorphism of position-effect variegation (PEV) on the white(mottled4) locus in RE strains. Our results suggest a model of regulation in which permissivity could depend on the chromatin state and on the hobo vestigial sequences.
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