Male-specific hexokinase functions as a seminal fluid protein to enhance insect fitness

Abstract

A growing body of evidence has highlighted the vital roles of male-specific seminal fluid proteins (SFPs) in animal sexual selection and reproduction. SFPs were proved to function as central mediators of reproductive fitness by interacting with female-derived molecules to modulate pivotal reproductive processes such as sperm competition, female receptivity, ovulation, and oogenesis. However, the underlying mechanisms of SFPs remain unclear. The present study reports on the hexokinase (hk) family of genes, specifically two members (hk1 and hk2), in the Ophraella communa genome. While hk1 was expressed in multiple tissues and did not affect fecundity, hk2 was specifically expressed in male testes and functioned as a novel and conserved SFP to enhance fertility. Furthermore, HK2 activated the expression of an Apolipophorin-like (Ap-like) gene, which is essential for beetle reproduction. The Ap-like gene activated the expression of triacylglycerol lipase (TGL), resulting in a change in the triglyceride content, which consequently affected fertility. These findings highlight a novel role of an animal HK family in SFP function. Moreover, the newly identified HK/Ap-like/TGL pathway provides new insights for future research on the SFP evolution theory.