Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets

Authors: BURNS-DUNN, SAMUEL - Western Sydney University; MORTYS, TASSIE - Western Sydney University; HOUSE, CLARISSA - Western Sydney University; MITCHELL, CHRISTOPHER - University Of Exeter; Duffield, Kristin; FOQUET, BERT - Illinois State University; SADD, BEN - Illinois State University; SAKALUK, SCOTT - Illinois State University; HUNT, JOHN - Western Sydney University

Submitted to: Proceedings of the Royal Society of London: Biological Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/3/2024
Publication Date: 7/3/2024
Citation: Burns-Dunn, S., Mortys, T., House, C.M., Mitchell, C., Duffield, K.R., Foquet, B., Sadd, B.N., Sakaluk, S.K., Hunt, J. 2024. Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets. Proceedings of the Royal Society of London: Biological Sciences. https://doi.org/10.1098/rspb.2024.0804.
DOI: https://doi.org/10.1098/rspb.2024.0804

Interpretive Summary: Across many spider and insect taxa, males provide females with a nuptial gift (i.e., non-sperm material) during mating. Nuptial gifts come in many forms, including captured prey items, or as a large gelatinous mass in the case of many crickets. Traditionally, nuptial gifts were thought to provide benefits to the female (e.g., nutrition), but there is growing evidence that some gifts can provide little to no benefit or even be detrimental to the paired female. The latter scenario suggests that there is sexual conflict over the evolution of nuptial gifts in some species. Here, we assessed the role that sexual conflict plays in the evolution of nuptial gifts in the decorated cricket, Gryllodes sigillatus. Using experimental evolution, we exposed populations to either elevated or reduced sexual conflict via altered sex ratios to either male-biased (high sexual conflict) or female-biased (low sexual conflict). After 25 generations, we found that males from the high sexual conflict lines (male-biased) produced heavier and more manipulative nuptial gifts compared to males from low sexual conflict lines (female-biased). These heavier and more manipulative gifts resulted in females feeding for longer and thus fertilizing more eggs with sperm from male-biased populations males. Together, these results demonstrate that sexual conflict plays a central role in the evolution of nuptial gifts in this cricket species. Moreover, because G. sigillatus is a species of economic importance (e.g., as a feed insect), this basic research could inform breeding efforts to optimizing favorable commercial traits.

Technical Abstract: The evolution of nuptial gifts has traditionally been considered a harmonious affair, providing benefits to both mating partners. There is growing evidence, however, that receiving a nuptial gift can be actively detrimental to the female. In decorated crickets (Gryllodes sigillatus), males produce a gelatinous spermatophylax that enhances sperm transfer but provides little nutritional benefit and hinders female post-copulatory mate choice. Here, we examine the sexually antagonistic coevolution of the spermatophylax and the female feeding response to this gift in G. sigillatus maintained in experimental populations with either a male-biased or female-biased adult sex ratio. After 25 generations, males evolving in male-biased populations produced heavier spermatophylaxes with a more manipulative combination of free amino acids than those evolving in female-biased populations. Moreover, when the spermatophylax originated from the same selection regime, females evolving in male-biased populations always had shorter feeding durations than those evolving in female-biased populations, indicating the evolution of greater resistance. Across populations, female feeding duration increased with the mass and manipulative combination of free amino acids in the spermatophylax, suggesting sexually antagonistic coevolution. Collectively, our work demonstrates a key role for interlocus sexual conflict and sexually antagonistic coevolution in the mating system of G. sigillatus.