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

Sara Bellinvia,Oliver Otti,Susan Mbedi,Paul R Johnston

doi:10.1098/rspb.2020.0302

Abstract

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.

Highlights

We sequenced 643 samples from bedbug reproductive organs or cuticle via 16S rRNA amplicon sequencing to characterize the composition of the genital microbiomes and investigate the effect of mating
We sampled the cuticle from both sexes, the external intromittent organ and the internal sperm vesicles and seminal fluid vesicles from males and the sperm-receiving organ, the ovaries and the haemolymph, which are all internal female organs
Multiple comparisons showed that the composition differed between the cuticle and the internal reproductive organs of both sexes

Summary

Introduction

We collected different reproductive tissues and cuticle samples from both sexes (n = 10 ± 0 per mating status, organ, sex and population; mean ± s.d.; see electronic supplementary material, table S1). We analysed the differences in microbiome composition between internal reproductive organs (sperm and seminal fluid vesicles of males; mesospermalege, haemolymph and ovaries of females), external reproductive organs (male paramere) and cuticle with a PERMANOVA (999 permutations, vegan package [59]) followed by a multilevel pairwise comparison using pairwise PERMANOVAs ( pairwiseAdonis package [58]) and Benjamini–Hochberg adjusted p-values. Compositional differences of genital microbiomes from virgin and mated bedbugs were analysed with a PERMANOVA with the fixed effects population, organ, mating status and their interactions. Non-significant interactions were removed to analyse the main effects, which improved the AIC

Results and discussion

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Methods