Dichotomous sperm in Lepidopteran insects: a biorational target for pest management

Abstract

Lepidoptera are unusual in possessing two distinct kinds of sperm, regular nucleated (eupyrene) sperm and anucleate (apyrene) sperm (‘parasperm’). Sperm of both types are transferred to the female and are required for male fertility. Apyrene sperm play ‘helper’ roles, assisting eupyrene sperm to gain access to unfertilized eggs and influencing the reproductive behavior of mated female moths. Sperm development and behavior are promising targets for environmentally safer, target-specific biorational control strategies in lepidopteran pest insects. Sperm dimorphism provides a wide window in which to manipulate sperm functionality and dynamics, thereby impairing the reproductive fitness of pest species. Opportunities to interfere with spermatozoa are available not only while sperm are still in the male (before copulation), but also in the female (after copulation, when sperm are still in the male-provided spermatophore, or during storage in the female’s spermatheca). Biomolecular technologies like RNAi, miRNAs and CRISPR-Cas9 are promising strategies to achieve lepidopteran pest control by targeting genes directly or indirectly involved in dichotomous sperm production, function, or persistence.

Differential gene expression underpinning the production of distinct sperm morphs in the wax moth Galleria mellonella

“…Interestingly, our RNA-seq analysis found a higher number of upregulated genes in pupal spermatocytes compared to larval, which contrasts with previous findings that apyrene sperm possess a less diverse proteome [10]. It also contrasts with the hypothesis that apyrene sperm present a functionally streamlined version of a eupyrene ancestor sperm present early in the lineage when dichotomous spermatogenesis evolved [2]. While some of the differences could be species-specific, we note that Whittington et al [10] investigated mature sperm proteomes, whereas we have focused on the earlier spermatocyte transcriptome [10].…”

“…With the importance of biodiversity becoming increasingly prevalent in the public consciousness, innovative solutions are required to effectively target these pest populations. Seth et al [2] recently proposed the presence of infertile apyrene sperm as a potential 'Achilles heel' to specifically target lepidopteran pests [2]. If one could engineer a strain that made normal apyrene sperm, but lacked eupyrene sperm, they should have good viability, mating competitiveness and induction of post-mating responses and yet be fully sterile.…”

Differential gene expression underpinning production of distinct sperm morphs in the wax mothGalleria mellonella

“…With the importance of biodiversity becoming increasingly prevalent in the public consciousness, innova)ve solu)ons are required to effec)vely target these pest popula)ons. Seth et al (2023) recently proposed the produc)on of infer)le apyrene sperm as a poten)al 'Achilles heel' to specifically target Lepidopteran pests (2).…”

“…With the importance of biodiversity becoming increasingly prevalent in the public consciousness, innovative solutions are required to effectively target these pest populations. Seth et al (2023) recently proposed the production of infertile apyrene sperm as a potential ‘Achilles heel’ to specifically target Lepidopteran pests (2). Our data set provides a resource to mine to investigate novel genes implicated in sperm differential morphogenesis, and specifically target genes involved in apyrene sperm development.…”

“…Each spermatogonium is enveloped by somatic cyst cells that form a squamous epithelium within which the germline cells differentiate. In Lepidoptera each male makes two distinct sperm types, a phenomenon known as sperm heteromorphism (see (1, 2) for detailed reviews). Each ejaculate contains both fertilising eupyrene sperm and non-fertilising apyrene sperm.…”