Female bed bugs (<i>Cimex lectularius</i>L) anticipate the immunological consequences of traumatic insemination via feeding cues

Siva‐Jothy, Michael T.; Zhong, Weihao; Naylor, Richard; Heaton, Louise L; Hentley, William T.; Harney, Ewan

doi:10.1073/pnas.1904539116

Cited by 26 publications

(21 citation statements)

References 39 publications

(56 reference statements)

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“…While our results do not refute this hypothesis, they are also consistent with C. maculatus females being “primed” for harmful mating and that PO activity in females initially decreases post mating as a result of wound healing but is then quickly restored. Such female anticipatory immunity activation has been observed in Drosophila (117, 118) and bed bugs (119).…”

Section: Discussionmentioning

confidence: 74%

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Bagchi

Corbel

Khan

et al. 2020

Preprint

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Sexual dimorphism in immunity is believed to reflect sex-differences in trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental data linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males as a result of sex-biased expression of genes in the proPO activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (relative to natural polygamy) rapidly decreases female (but not male) PO activity. The evolution of decreased PO in monogamous females was accompanied by increased tolerance to bacterial infection unrelated to mating. This implies that female responses to costly mating may trade off with other aspects of immune defence. Finally, female (but not male) PO activity show correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Our results thus provide a proximate and ultimate understanding of the links between sexual selection and sexual dimorphism in immunity.

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Section: Discussionmentioning

confidence: 74%

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Bagchi

Corbel

Khan

et al. 2020

Preprint

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“…However, lysozyme-injected females and females exposed to prolonged mating were less likely to suffer reproductive senescence, possibly reflecting complex interactions between deleterious effects of insemination (possibly mediated by bacteria) and beneficial effects (e.g., courtship feeding) [71]. These patterns may be partly explained by the recent discovery that females ramp up their immune system in expectation of traumatic insemination (i.e., following a blood meal) [81].…”

Section: The Reproductive Microbiome and Sexual Conflictmentioning

confidence: 99%

The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation

Rowe

Veerus

Trosvik

et al. 2020

Trends in Ecology & Evolution

110

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All multicellular organisms host microbial communities in and on their bodies, and these microbiomes can have major influences on host biology. Most research has focussed on the oral, skin, and gut microbiomes, whereas relatively little is known about the reproductive microbiome. Here, we review empirical evidence to show that reproductive microbiomes can have significant effects on the reproductive function and performance of males and females. We then discuss the likely repercussions of these effects for evolutionary processes related to sexual selection and sexual conflict, as well as mating systems and reproductive isolation. We argue that knowledge of the reproductive microbiome is fundamental to our understanding of the evolutionary ecology of reproductive strategies and sexual dynamics of host organisms. The Microbiome Revolution and the Reproductive MicrobiomeAnimals and plants live and evolve in a world dominated by microbes, and host a diversity of microbial communities in and on their bodies. A recent explosion in research on host-associated microbial communities (i.e., microbiota and/or microbiomes, see Glossary) is revolutionising biology. While earlier research typically considered microorganisms from a pathological perspective, it is now widely accepted that the relationship between host and microbes spans a continuum, from detrimental to beneficial. Through their influence on host health, physiology, development, and behaviour [1,2], microbiomes can be seen as an integral part of the host phenotype, and potentially also the host genome (e.g., the hologenome concept [3], but see [4]). While considerable attention has been paid to the role of oral, skin, and gut microbiomes in host ecology, evolution, and fitness, less is known about the reproductive microbiome (Box 1). This is surprising given longstanding knowledge of microbes in male and female reproductive systems (e.g., [5]), most notably in the context of sexually transmitted infections (STIs) [6], and more recent DNA-sequencing studies demonstrating the presence of dynamic microbial communities in reproductive tissues [7], especially the vagina [8,9]. Thus, the reproductive microbiome represents an outstanding challenge in the study of host-associated microbial communities.

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“…The high number of haemocytes [46] able to phagocytose bacteria [78] in this organ might stabilize its microbiome and protect against invading bacteria. In addition, lysozyme in the seminal fluid of males [79] and in the mesospermalege produced in anticipation of mating [80] could help to reduce invading bacteria. Furthermore, endosymbionts have been shown to interact with invading microbes [42][43][44][45] and might help to control non-resident bacteria in the genital microbiomes.…”

Section: (Ii) Prevalence and Abundance Changesmentioning

confidence: 99%

Mating changes the genital microbiome in both sexes of the common bedbug Cimex lectularius across populations

et al. 2020

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Many bacteria live on host surfaces, in cells and in specific organ systems. In comparison with gut microbiomes, the bacterial communities of reproductive organs (genital microbiomes) have received little attention. During mating, male and female genitalia interact and copulatory wounds occur, providing an entrance for sexually transmitted microbes. Besides being potentially harmful to the host, invading microbes might interact with resident genital microbes and affect immunity. Apart from the investigation of sexually transmitted symbionts, few studies have addressed how mating changes genital microbiomes. We dissected reproductive organs from virgin and mated common bedbugs, Cimex lectularius L., and sequenced their microbiomes to investigate composition and mating-induced changes. We show that mating changes the genital microbiomes, suggesting bacteria are sexually transmitted. Also, genital microbiomes varied between populations and the sexes. This provides evidence for local and sex-specific adaptation of bacteria and hosts, suggesting bacteria might play an important role in shaping the evolution of reproductive traits. Coadaptation of genital microbiomes and reproductive traits might further lead to reproductive isolation between populations, giving reproductive ecology an important role in speciation. Future studies should investigate the transmission dynamics between the sexes and populations to uncover potential reproductive barriers.

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Female bed bugs (Cimex lectulariusL) anticipate the immunological consequences of traumatic insemination via feeding cues

Cited by 26 publications

References 39 publications

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation

Mating changes the genital microbiome in both sexes of the common bedbug Cimex lectularius across populations

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