The transfer of male cuticular hydrocarbons provide a reliable cue of the risk and intensity of sperm competition in decorated crickets

Authors: HOUSE, CLARISSA - Western Sydney University; Duffield, Kristin; RAPKIN, JAMES - Western Sydney University; SAKALUK, SCOTT - Illinois State University; HUNT, JOHN - Western Sydney University

Submitted to: Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/23/2024
Publication Date: N/A
Citation: N/A

Interpretive Summary: The decorated cricket is increasingly used as a sustainable source of protein for animals and humans and understanding its reproduction biology is essential for breeding and rearing efforts. This study assessed male cricket fertility focusing on competition for egg fertilization (i.e., paternity). Female crickets mate with many males over their lifetime and store sperm from each mating for extended periods of time. This scenario presents intense competition for egg fertilization between males. Because males attempt to produce as many offspring as possible, it is expected that males should adjust their investment of sperm (e.g., the total number) for each female mate based on their perception of competition risk, or how many mates she has had previously. This study investigated whether males can determine the number of mates a female has had previously by smelling her cuticular hydrocarbons (CHCs). CHCs are long-chained hydrocarbons found on the bodies of nearly all insects and can be physically transferred from one individual to another during physical contact, including mating. By counting the number of sperm males transferred to virgin females that were treated with CHCs derived from varying number of males, we found that males transferred more sperm to females treated with CHCs compared to control females. This study demonstrates that decorated cricket males use the smell of CHCs of females to adjust the number of sperm transferred during mating. These findings can be used to optimize the breeding and mass production of these economically important insects.

Technical Abstract: Sperm competition theory predicts that males should increase the number of sperm in their ejaculate when the risk of sperm competition increases but decrease sperm number when the intensity of sperm competition increases. Here we examine whether male decorated crickets (Gryllodes sigillatus) use the cuticular hydrocarbons (CHCs) transferred to females by rival males to assess the risk and intensity of sperm competition and to adjust their ejaculate accordingly. Virgin females perfumed with CHCs extracted from one, three or five males could be distinguished chemically, providing males with a reliable cue of the risk and intensity of sperm competition. Males mated to virgin females perfumed with these CHC extracts or to unperfumed females produced more sperm as the risk of sperm competition increased, whereas sperm number decreased linearly with the intensity of sperm competition (i.e., number of competing males). Similarly, an increase in the risk of sperm competition risk led to increased investment in an important non-sperm component of the ejaculate, the spermatophylax, a gelatinous mass consumed by the female after mating that promotes sperm transfer. However, both the mass of spermatophylax and its attractiveness (assessed by its amino acid content) decreased only from the one- to the three-male CHC perfuming treatment. Moreover, only the mass of the spermatophylax from the five-male CHC treatment was lower than the unperfumed control. Our results therefore demonstrate that both sperm and non-sperm components of the male ejaculate respond to the risk and intensity of sperm competition in different ways and that CHCs provide an important cue to males as to how to strategically tailor their ejaculate.