Motility and dynamics of eupyrene and apyrene sperm in the spermatheca of the monandrous swallowtail butterfly Byasa alcinous

Abstract

Lepidopteran males produce two sperm types: nucleated eupyrene sperm and non-nucleated apyrene sperm. Although apyrene sperm are infertile, both sperm types migrate from the spermatophore to the spermathecal after copulation. As a dominant adaptive explanation for migration of apyrene sperm in polyandrous species, the cheap filler hypothesis suggests that the presence of a large number of motile apyrene sperm in the spermatheca reduces female receptivity to re-mating. However, apyrene sperm are also produced in males of the monandrous swallowtail butterfly Byasa alcinous Klug. To identify the role of apyrene sperm in these males, the present study examines the number of spermatozoa produced and transferred and the dynamics and motility of spermatozoa in the spermatheca for each type of sperm. Apyrene sperm represents approximatey 89% of the sperm produced and transferred, which is comparable to polyandrous species. Two-day-old males transfer approximately 17 000 eupyrene and 230 000 apyrene spermatozoa to a spermatophore; approximately 5000 eupyrene and 47 000 apyrene spermatozoa arrive at the spermatheca. Eight days after copulation, most eupyrene spermatozoa remain in the spermatheca and a quarter of them are still active. However, the number of apyrene spermatozoa decreases and those remaining lose their motility after the arriving at the spermatheca. Consequently, 8 days after copulation, no motile apyrene sperm are found. The high proportion of apyrene sperm in the spermatophore, as well as in sperm migration, suggests that the production and migration of apyrene sperm is not simply an evolutionary vestigial trait. The possible functions of apyrene sperm in monandrous species are discussed.

Dimorphic sperm formation by Sex-lethal

“…These results indicate that apyrene sperm are necessary for eupyrene sperm migration from the bursa copulatrix to the spermatheca. In recent years, delayed female remating has been a dominant explanation for apyrene sperm function in lepidopteran insects (20, 31). In agreement, storage of large numbers of apyrene sperm in the spermatheca prevented remating in the green-veined white ( P. napi ) (23).…”

“…In contrast, our results clearly indicate that apyrene sperm are essential for fertilization in B. mori . However, because the delayed female remating hypothesis cannot apply to monandrous species (31), this cannot be the only function of apyrene sperm in lepidopteran insects. Accordingly, the present study emphasizes the importance of nonfertile sperm in fertilization.…”

Destination of apyrene sperm following migration from the bursa copulatrix in the monandrous swallowtail butterfly Byasa alcinous

“…A study of the polyandrous green-veined white butterfly, Pieris napi, by Cook and Wedell supports this hypothesis 11 : females that store a larger number of apyrene sperm show a lower receptivity for re-mating. However, this hypothesis is more controversial in other species [12][13][14] . On the other hand, apyrene sperm is necessary for complete dissociations of eupyrene sperm bundles in Bombyx mori 9 .…”

“…Sperm dynamics in the spermatheca have previously been reported in many polyandrous and a few monandrous species. Apyrene sperm is known to arrive in the spermatheca earlier than eupyrene sperm in both polyandrous 19 and monandrous species 13 , and the migration of both sperm types ends approximately 1–2 days after mating 20 . While the eupyrene sperm is maintained in the spermatheca until oviposition, the number of apyrene sperm decreases with time 21 .…”

Field and Laboratory Studies on the Ecology, Reproduction, and Adult Diapause of the Asian Comma Butterfly, Polygonia c-aureum L. (Lepidoptera: Nymphalidae)

“…Furthermore, in polyandrous lepidopteran species, the presence of many apyrene sperm in the spermatheca reduces the receptivity of the female to remating [27]. In the monandrous swallowtail butterfly Byasa alcinous (Klug), virgin males always transfer ejaculate that has a high proportion of apyrene sperm [28], as also occurs in some polyandrous species such as Eureuma mandarina (de I’Orza) [29] and Papilio xuthus L. [30].…”