Partitioning the effects of mating and nuptial feeding on the microbiome in gift-giving insects

Authors: SMITH, CHAD - University Of Texas; Srygley, Robert; DIETRICH, EMMA - University Of Texas; MUELLER, ULRICH - University Of Texas

Submitted to: Environmental Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2016
Publication Date: 4/1/2017
Citation: Smith, C.C., Srygley, R.B., Dietrich, E.I., Mueller, U.G. 2017. Partitioning the effects of mating and nuptial feeding on the microbiome in gift-giving insects. Environmental Microbiology Reports. 9(2):104-112. doi:10.1111/1758-2229.12506.

Interpretive Summary: We investigated the guts of female Mormon crickets and decorated crickets to determine if sperm transfer and nuptial gifts provided by males altered their microbial communities. Because Mormon cricket males donate a larger nuptial gift (~19% body weight) to females than the decorated crickets (~5% body weight), we expected that Mormon cricket females would be more likely to have their microbial communities altered by the nuptial gift. Surprisingly, mating, but not nuptial gift consumption, affected the composition of the gut microbiome, and only in Mormon crickets. Mated Mormon crickets had more lactic acid bacteria, known for their beneficial effects on nutrition and immunity, than unmated females. Dietary protein did not alter the composition of the gut microbiome of decorated crickets, indicating insensitivity of their gut microbes to available protein, and potentially explaining why nuptial gift consumption did not alter the gut microbial community. Mating is often investigated in pathogen transmission, but we conclude that it may also promote beneficial gut bacteria. Effects of the shift in the microbial community of Mormon crickets on their resistance to natural pathogens and microbial control remain to be investigated.

Technical Abstract: Mating is a ubiquitous social interaction that has the potential to influence the microbiome by facilitating transmission, modifying host physiology, and in species where males donate nuptial gifts to females, altering diet. We manipulated mating and nuptial gift consumption in two insects that differ in nuptial gift size, the Mormon cricket Anabrus simplex (~19% male body weight) and the decorated cricket Gryllodes sigillatus (~5% male body weight), with the expectation that larger gifts are more likely to affect the gut microbiome. Surprisingly, mating, but not nuptial gift consumption, affected the composition of the gut microbiome, and only in Mormon crickets. The change in composition was due to higher abundances of lactic-acid bacteria in mated females, a taxon known for their beneficial effects on nutrition and immunity. Reproductive tissues lacked bacteria in both species and protein supplementation did not affect the gut microbiome in decorated crickets, suggesting that sexual transmission is unlikely and that insensitivity of gut microbes to dietary protein could contribute to the lack of an effect of nuptial gift consumption. Our study provides experimental evidence that sexual interactions can affect the microbiome and suggests mating can promote beneficial gut bacteria.