Female immunity in response to sexually transmitted opportunistic bacteria in the common bedbug Cimex lectularius

Abstract

Besides typical sexually transmitted microbes, even environmental, opportunistic microbes have been found in copulatory organs of insects and even humans. To date, only one study has experimentally investigated the sexual transmission of opportunistic microbes from male to female insects, whereas nothing is known about the transmission from females to males. Even if opportunistic microbes do not cause infection upon transmission, they might eventually become harmful if they multiply inside the female. While the immune system of females is often assumed to target sexually transmitted microbes, most studies ignore the role of mating-associated opportunistic microbes. Variation in immunity between populations has been linked to parasite or bacteria prevalence but no study has ever addressed between-population differences in immune responses to sexually transmitted opportunistic microbes. We here show that bacteria applied to the copulatory organs of common bedbugs, Cimex lectularius, are sexually transmitted to the opposite sex at a high rate, including the transmission from female to male. Bacterial growth in the female sperm-receiving organ was inhibited over the first hours after introduction, but after this initial inhibition bacterial numbers increased, suggesting a shift of investment from immune defence towards reproduction. However, 24 h after the injection of bacteria, male components, or saline as a control, the sperm-receiving organ showed lysozyme-like activity and inhibited the growth of Gram-negative and Gram-positive bacteria in vitro, potentially to mop up the remaining bacteria. Contrasting our prediction, neither bacterial growth nor immune responses differed between populations. Future studies should link transmission dynamics, immune responses and fitness effects in both sexes. Experimental manipulation of environmental bacteria could be used to investigate how transmission frequency and toxicity of sexually transmitted opportunistic microbes shapes bacteria clearance and immune responses across populations.