In vitro antimicrobial sperm protection by an ejaculate‐like substance

Abstract

Summary Ejaculate substances are hugely diverse among and within species. The functional significance of this diversity has been little studied except for a few accessory gland proteins. These studies suggest that ejaculate components evolve mainly by sexual selection, that is, sperm competition, male–female co‐evolution or by female choice for paternal investment. However, male benefits of protecting sperm from microbial harm, that is, antimicrobial ejaculate protection, has received little attention in the evolutionary literature, while it has been discussed in the human and livestock literature. Here, we examine in the common bedbug, Cimex lectularius, the two basic components of the antimicrobial ejaculate protection hypothesis: 1) microbes damage sperm cells and 2) antimicrobial ejaculate substances prevent such microbe‐induced sperm damage. We found that environmental microbes, which are sexually transmitted in bedbugs, induce sperm mortality. Sperm mortality was high (increased 40% compared with controls without bacteria) and very rapid (within 10 min) in vitro. Consistent with the antimicrobial sperm protection hypothesis, a lysozyme dose equivalent to the amount of antibacterial lysozyme‐like activity that is transferred in the seminal fluid during a single mating was sufficient to reduce sperm mortality to control levels. While this result is not necessarily predicted by the paternal investment hypothesis, it is plausible that female benefits of male immune substances may evolve under the male–female co‐evolution hypothesis. We found that weekly physiological lysozyme doses equivalent to the observed lysozyme‐like activity in seminal fluid benefit females to some extent, indicating that immune‐active ejaculate substances may have a secondary gift function and may release females from a trade‐off between reproduction and immunity. Lysozyme seems to stimulate early egg‐laying above the female optimum and later cause earlier reproductive senescence, which is not consistent with the idea of an overall direct benefit but is consistent with the idea that males transfer manipulative substances to the females. Our data are consistent with antimicrobial sperm protection. They support the idea of a naturally selected origin of ejaculate components and provide a mechanistically well‐defined pathway how sexual selection can affect ejaculate composition via antimicrobial sperm protection. As sperm and microbes frequently encounter each other in many species, antimicrobial sperm protection may be a common phenomenon and has the potential to inform models of male and female co‐evolution and biological diversification.