Eupyrene and Apyrene Sperm: Dichotomous Spermatogenesis in Lepidoptera

A study of meiosis and spermiogenesis in the testicular lobes of Antiteuchus tripterus (Heteroptera: Pentatomidae)

“…The regular production of cytogenetically differentiated spermatozoa was first described in gastropods in 1836 (Seibold, 1836, cited in Hodgson, 1977, and is now known to occur in several invertebrates, such as spiders (Rosati et al, 1970), centipedes (Jamieson, 1986) and many insects (Sivinski, 1980). Moths and butterflies, for example, produce both nucleate and anucleate spermatozoa; and some bedbugs and beetles produce spermatozoa with a very variable number of chromosomes (Swallow & Wilkinson, 2002;Friedländer et al, 2005). Morphological variations may also affect spermatozoal size, as observed in some bedbugs and beetles, length, as in some flies and shape, as in some wasps (Swallow & Wilkinson, 2002).…”

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis

“…nebenkern) in flagellum development 271 and presence of mitochondrial derivatives in mature spermatozoa (Fig 1a-b) [38]. During lepidopteran 272 spermatogenesis, the nebenkern divides to form two derivatives, which flank the axoneme during 273 elongation; ultrastructure and size of these derivatives varies greatly between species and between the 274 two sperm morphs [7]. In Drosophila, the nebenkern acts as both an organizing center for microtubule 275 polymerization and a source of ATP for axoneme elongation, however it is unclear to what extent these 276 structures contribute to energy required for sperm motility.…”

“…288 Molecular Function GO analysis revealed an enrichment of oxidoreductase proteins acting on 289 NAD(P)H (p = 7.06E-19), as well as more moderate enrichments in several categories relating to 290 peptidase activity or regulation of peptidase activity (data not shown). The broad representation of 291 proteins involved in proteolytic activity is worthy of discussion, not solely because these classes of 292 proteins are abundant in other sperm proteomes, but also because proteases are involved in the 293 breakdown of the fibrous sheath surrounding Lepidoptera eupyrene sperm upon transfer to the female 294 [7]. This process has been attributed to a specific ejaculatory duct trypsin-like arginine C-endopeptidase 295 (initiatorin) in the silkworm (B. mori) [41] and a similar enzymatic reaction is needed for sperm 296 activation in Manduca [42].…”

“…Third, the ratio or eupyrene to apyrene varies substantively across Lepidoptera but is 64 relatively constant within species, including several cases where apyrene comprise up to 99% of the 65 sperm produced [7]. While variation in the relative production of each sperm morph is not in itself 66 incompatible with stochastic processes, such as drift, it is nearly impossible to reconcile the 67 disproportionate investment in apyrene without acknowledging that they contribute in some 68 fundamental way to reproductive fitness.…”

“…Interestingly, cessation of calling appears to be 90 governed by molecular factors present in sperm or seminal fluid [12] and, as a consequence, non-virgin 91 females rarely remate. Despite these behavioral differences, the proportion of eupyrene and apyrene 92 produced is quite similar between these two species (~95-96%) [7,13]. Thus, our focus on Monarch is 93 motivated both by their disparate, polyandrous mating system and their utility as a representative 94 butterfly species for comparative analyses with Manduca.…”