Disentangling host-parasite and male-female coevolutionary effects on host fitness
Final Report Abstract
Sexual reproduction is a highly complicated process shaped by the need to optimise reproductive investment, which can differ and evolve antagonistically between the sexes. Sexual reproduction is also intimately linked with immunity through a variety of means. Combining these seemingly disparate biological functions has led to the emergence of the new field of reproductive immunity. The relationship between reproduction and immunity is likely affected by the mating system and the degree of sexual conflict. The rapid evolution of male and female reproductive traits has long been regarded as driven only by sexual selection. However, 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 microbes can eventually cause disease or death, but they can also reduce reproductive success due to their spermicidal activity or indirectly by activating the female immune system, resulting in tissue and sperm damage. Transmitted opportunistic microbes might disturb the microbial communities inhabiting the reproductive organs, activating costly immune responses. Host populations are likely exposed to different environmental microbes as well as genital microbiomes. If hosts and microbes are locally adapted, host populations likely differ in the type and strength of the immune defence. Our work funded by the DFG provides new results highlighting the importance of environmental factors affecting reproduction and immunity. Apart from human studies, we present the first genital microbiomes. The variation in genital microbiomes across populations suggests local adaptation, giving them a potential role in speciation. Sperm also seems to adapt to microbes, making this statement even more robust. Characterising the genital microbiomes in bedbugs has shown that microbes are sexually transmitted during almost every mating. Also, mating changes the bacterial communities in reproductive organs. We assume sexually reproducing organisms are regularly exposed to invading microbes, and therefore males and females should be selected for defending themselves against sexually transmitted opportunistic infections. Next to our earlier studies on male sperm protection via an antibacterial ejaculate substance, we found evidence within this funding period that females defend themselves and the sperm they received by inhibiting the growth of opportunistic microbes inside their sperm-receiving organ during the important sperm passage from this organ to the ovaries and sperm storage organs. This provides additional support for an important link between mating and immunity. The regular occurrence of sexual transmission, together with the absence of a populationspecific reproductive immune response, might indicate high or inevitable fitness costs that must be paid to maintain reproduction. In conclusion, our project gives an overview of how host-microbe interactions affect sexual reproduction and highlights the importance of reproductive ecology and immunity and a role in reproductive isolation. With this project, we have established a model system in which we can now continue to ask exciting new research questions within the fields of reproductive immunity and sperm ecology.
Publications
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2017. Regular wounding in a natural system: bacteria associated with reproductive organs of bedbugs and their quorum sensing abilities. Frontiers in Immunology 8: 1855
Otti O, Deines P, Hammerschmidt K, Reinhardt K
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2019. Do bacteria change their language when they enter the body through wounds? Answers from bedbug experiments. Frontiers for Young Minds 7: 1
Otti O, Deines P, Hammerschmidt K, Reinhardt K
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2020. Bacterial communities of the reproductive organs of virgin and mated common bedbugs, Cimex lectularius. Ecological Entomology 45: 142-154
Bellinvia S, Johnston PR, Reinhardt K, Otti O
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2020. Female immunity in response to sexually transmitted opportunistic bacteria in the common bedbug Cimex lectularius. Journal of Insect Physiology 123: 104048
Bellinvia S, Spachtholz A, Borgwardt I, Schauer B, Otti O
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2020. Mating changes the genital microbiome in both sexes of the common bedbug Cimex lectularius. Proceedings of the Royal Society London B 287: 20200302
Bellinvia S, Johnston PR, Mbedi S, Otti O
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2020. Sexual reproduction and immunity. In: eLS. John Wiley & Sons, Ltd: Chichester
Barribeau S, Otti O
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2020. Transmission, tropism and biological impacts of torix Rickettsia in the common bed bug Cimex lectularius (Hemiptera: Cimicidae). Frontiers in Microbiology 11:608763
Thongprem P, Evison S, Hurst GDD, Otti O
