Transfer, subsequent movement, and fate of sperm in the tobacco hornworm moth, Manduca sexta

Abstract

During mating in the Lepidoptera (moths and butterflies), sperm are passed to the female via a copulation in which the male transfers a large and often complex spermatophore over the major part of an hour or more. Subsequently, over the course of an hour or often considerably more, the sperm exit the spermatophore and travel over a relatively complex route to the spermatheca, where the sperm are stored and then used as the eggs are laid. The process of spermatophore formation and migration of sperm in the female has been described in many Lepidoptera, but the mechanics involved have received less attention. Understanding these is important in discerning the relative roles of males and females in determining the outcome of matings. We describe how the spermatophore is formed, how the sperm migrate in the female, and the fate of the sperm in the spermatheca of the tobacco hornworm moth, Manduca sexta. We found that sperm movement from the spermatophore relied upon motility of the sperm, but further movement of the sperm to the spermatheca was dependent on female muscular action. After arriving in the spermatheca, the anucleate parasperm (apyrene sperm) separated into the lateral pouch of the spermatheca (lagena) and disappeared over 7 days, whereas the eusperm (eupyrene sperm) persisted in the central lumen of the spermatheca (utriculus). The relative persistence of these two sperm types could shed some light on what determines the proclivity of females to remate. Elucidation of these physiological mechanisms contributes to an understanding of the mechanisms of female choice and male competition in Lepidoptera.

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect

“…Previous studies on E. kuehniella show that adult males increase the apyrene-eupyrene ratio in response to the presence of rivals [10] but male larvae reduce the ratio after exposed to larval cues [19]. These may be ascribed to the fact that spermatogenesis of apyrenes and eupyrenes occurs at different stages of insects [53,73] and they have different functions in reproduction [56][57][58][59][60], allowing adults to increase investment in apyrene and larvae to trade-off apyrene for more eupyrene. However, the current study on pupae demonstrates that the apyrene-eupyrene ratio was about 5:1 with no significant difference between treatments.…”

“…Apyrenes may function to delay female remating [55,56] protect eupyrenes in female reproductive tract [57] or enable eupyrenes to migrate to the spermatheca [58]. More recent studies suggest that the role of apyrenes may be completed after both types of sperm arrive at the spermatheca [59,60]. The apyrene to eupyrene ratio remains consistent under the food shortage during the larval stage [61] or environmental stress during the larval [62] and pupal stages [63].…”

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect

“…Previous studies on E. kuehniella show that adult males increase the apyrene-eupyrene ratio in response to the presence of rivals [10] but male larvae reduce the ratio after being exposed to larval cues [19]. These may be ascribed to the fact that spermatogenesis of apyrenes and eupyrenes occurs at different stages of insects [53,73] and they have different functions in reproduction [56][57][58][59][60], allowing adults to increase investment in apyrene and larvae to trade-off apyrene for more eupyrene. However, the current study on pupae demonstrates that the apyrene-eupyrene ratio was about 5:1 with no significant difference between treatments.…”

“…Apyrenes may function to delay female remating [55,56], protect eupyrenes in the female reproductive tract [57], or enable eupyrenes to migrate to the spermatheca [58]. More recent studies suggest that the role of apyrenes may be completed after both types of sperm arrive at the spermatheca [59,60]. The apyrene-to-eupyrene ratio remains consistent under food shortage during the larval stage [61] or environmental stress during the larval [62] and pupal stages [63].…”

The Functional Morphology of the Bursa Copulatrix of a Butterfly That Does Not Digest Spermatophores (Leptophobia aripa, Pieridae)

“…Genitalia terminology follows Klots [ 9 ]. Terminology of the spermatophore follows Mann [ 12 ], except for the spermatophore “corpus” which, in agreement with Drummond [ 13 ] and Hague et al [ 14 ], we call the “bulb” to avoid confusion with the “corpus bursae”.…”