Disentangling host-parasite and male-female coevolutionary effects on host fitness

Abstract

The rapid evolution of male and female reproductive traits has long been regarded as driven only by sexual selection. However, also natural selection, for instance mediated by parasites, can shape reproductive traits. Microbes are probably the most common parasite group and all animals are in constant contact with them. Besides microbes causing sexually transmitted diseases, opportunistic environmental bacteria seem to be sexually transmitted. Transmitted opportunistic microbes can eventually cause disease or death but they can also reduce reproductive success for example due to their spermicidal activity or indirectly by activating the female immune system resulting in tissue and sperm damage. In addition, transmitted opportunistic microbes might disturb the microbial communities inhabiting the reproductive organs, the genital microbiomes. Such disturbances could activate immune responses that are costly in terms of resources and might cause autoimmunity. Host populations are likely exposed to different environmental microbes or different microbe prevalences as well as differences in the composition of genital microbiomes. If hosts and environmental microbes and/or hosts and their genital microbiomes are locally adapted, host populations likely differ in the type of strength of immune defence. Unfortunately, to date little is known about the composition and mating-induced change of the genital microbiomes in insects and how the female immune system reacts to invading microbes. To characterise the genital microbiomes, I conducted two metagenomic studies based on the 16S rRNA gene of the bacteria present in and on the reproductive organs of the common bedbug (Cimex lectularius L.). By comparing the genital microbiomes of virgin and mated bedbugs of both sexes from four different populations, I found that genital microbiomes are organ-, sex-, and population-specific, indicating local adaptation. Differences in genital microbiomes might interfere with reproductive success if they lead to reproductive incompatibilities, and ultimately lead to speciation. Indeed, I found that mating-induced changes in the composition of the genital microbiomes are partly due to exchanges of bacterial strains during mating, indicating sexual transmission in both directions. Some of these sexually transmitted bacteria were opportunistic bacteria, i.e. bacteria from the cuticle. This indication was supported by my third study that investigated the transmission rate of opportunistic microbes and the growth rate and effect of such bacteria on the female immune system. Bacteria applied to the copulatory organs of males and females were transmitted to the opposite sex during mating in at least ninety percent of the cases, indicating that females are regularly threatened by sexually transmitted opportunistic microbes. Bacteria injected into the female paragenital sperm-receiving organ grew slowly within the first six hours, followed by a rapid growth within the next eighteen hours. The injection of bacteria but also the injection of ejaculate…