The transfer of male cuticular hydrocarbons provides 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: 9/1/2024
Citation: House, C.M., Duffield, K.R., Rapkin, J., Sakaluk, S.K., Hunt, J. 2024. The transfer of male cuticular hydrocarbons provides a reliable cue of the risk and intensity of sperm competition in decorated crickets. Evolution. https://doi.org/10.1093/evolut/qpae088.
DOI: https://doi.org/10.1093/evolut/qpae088

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: Theoretically, males should increase their ejaculate expenditure when the probability of sperm competition occurring (or risk) is high but decrease ejaculate expenditure as the number of competing ejaculates (or intensity) increases. Here we examine whether male decorated crickets (Gryllodes sigillatus) use cuticular hydrocarbons (CHCs) transferred to females by rival males at mating to assess the risk and intensity of sperm competition and adjust their ejaculate accordingly. Unmated females and those perfumed with CHCs extracted from one, three, or five males could be distinguished chemically, providing a reliable cue of the risk and intensity of sperm competition. In agreement with theory, males mating with these females increased sperm number with the risk of sperm competition and decreased sperm number with the intensity of sperm competition. Similarly, as the risk of sperm competition increased, males produced a larger and more attractive spermatophylax (an important non-sperm component of the ejaculate) but these traits did not vary with the intensity of sperm competition. 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 males with an important cue to strategically tailor their ejaculate.