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

Abstract

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 and sperm length influence the rate of mammalian spermatogenesis

“…It seems intuitively appealing that longer sperm will take longer to manufacture (Lü pold et al 2009); for example, there is evidence that the rate of spermatogenesis tracks strain-and species-specific variation in sperm size in nematodes (see LaMunyon & Ward (2002) and references therein). More generally, evidence for the substantial costs of spermatogenesis resulting from sperm size evolution comes from Drosophila, in which increasing sperm length delays male reproductive maturity (Pitnick et al 1995), increases resources required for sperm production and packaging (Pitnick 1996;Joly et al 2008) and selects for prudent male sperm-production strategies (Bjork et al 2007). Further work is needed to explore how selection on sperm numbers and sperm length combines to affect the evolution of testicular architecture (Schärer et al 2008;Lü pold et al 2009), and how the various features of the testis investigated to date are functionally integrated.…”

“…Sperm size and morphology is highly variable in the animal kingdom (see a review in Pitnick et al 2009), including in mammals (Gage 1998). The selective forces responsible for shaping sperm size evolution continue to be debated (see §4), but it seems likely that sperm of differing sizes will place different demands on the machinery of spermatogenesis (Schärer et al 2008;Lü pold et al 2009) and involve different time or resource costs (Pitnick et al 1995;Pitnick 1996;LaMunyon & Ward 2002;Joly et al 2008). If larger sperm take longer to produce, this may form the basis of an evolutionary trade-off between sperm size and numbers, with important theoretical implications for understanding the evolution of sperm competition phenotypes (see Pitnick 1996).…”

Coevolution of male and female reproductive structures in Drosophila

“…Sample sizes are given in parentheses Drosophilidae, which also exhibits the longest sperm of all animals (Joly et al 1995Pitnick et al 1995b). The driving force behind such rapid divergence in Drosophilid sperm morphology (Sivinski 1984;Joly et al 1989) is considered to be linked with the evolution of reproductive organs that manufacture sperm in males and receive them in females (Pitnick 1996;Pitnick et al 1999Pitnick et al , 2003Miller and Pitnick 2002;Joly et al 2008). Moreover, the testes warrant special consideration due to the potential influence that sexual selection may have on testicular architecture which drives sperm production (Schärer et al 2008;Ramm and Stockley 2009).…”

“…The least amount of variation is found in fishes and birds, the greatest level of divergence (among those animals that have been studied) is observed in the family Fig. 1 Box plots (median as the middle line, 25 and 75% quantiles as box boundaries, and 10 and 90% quantiles as whiskers) of sperm length (log) among different taxonomical groups (data from Joly et al 2008). The Drosophilidae family is represented by 11 genera, 5 subgenus, and 25 groups.…”

The evolutionary ecology of testicular function: size isn't everything

“…Many species of this genus produce giant sperm, reaching an extreme in the 58 mm long sperm of D. bifurca (Pitnick, Spicer & Markow, 1995b). The cost of producing such long sperm is substantial and morphologically well reflected (Pitnick & Markow, 1994;Pitnick, Markow & Spicer, 1995a), necessitating both longer testes (Pitnick, 1996) and specialised sperm-processing and storage structures (Joly, Luck & Dejonghe, 2008). Moreover, the spermatid elongation phase for the ca.…”