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

Abstract

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.

Selfish genetic elements and male fertility

“…For example, in humans, there is an association between the microbial community and sperm quality [84]. However, it remains unclear how these microbes influence sperm parameters or if this promotes their transmission (see [79] for review). Nonetheless, these impacts on male fertility have clear parallels with impacts of vertically transmitted SGEs.…”

The role of oxidative stress in postcopulatory selection

“…reviewed in [106]). Furthermore, leucocytes in the ejaculate, bacterial infection and inflammation of the male reproductive system are significant contributors to male infertility [31], and the role of oxidative stress and damage owing to these factors is an exciting emergent field [107,108].…”

Simplified model assumptions artificially constrain the parameter range in which selection at the holobiont level can occur

“…This simple alteration of VVD's model-assumptions leads to a broad parameter space in which a stable population of helper microbes is maintained despite their costly behavior, suggesting selection at the holobiont-level (Fig 2). Such a non-linear dependency of fitness on an underlying factor that can be influenced by the microbiome is not uncommon in the real world, stemming from physiological, ecological, or behavioral factors (2)(3)(4)(5). VVD's model may thus suggest the opposite conclusion from the one they reach, depending on the choice of fitness function.…”