Evidence That the Microbiota Counteracts Male Outbreeding Strategy by Inhibiting Sexual Signaling in Females

Chloe Heys,Hervé Colinet,Fiona Ingleby,Zenobia Lewis,Mark Prescott,Anne Lizé,Thomas A R Price

doi:10.3389/fevo.2018.00029

Abstract

The microbiota is increasingly being recognized as having important impacts on many host biological processes. However, evidence of its effects on animal communication and breeding strategy is lacking. In this three-factorial study, we show that females were more willing to mate with related males, with relatedness likely being assessed through the microbiota. By contrast, male mating investment is concurrently determined by both the relatedness and microbiota status of the female. When the microbiota in female Drosophila melanogaster is altered by an antibiotic, male investment in sperm number increased when mating with unrelated females compared to related ones. Contrastingly, the presence of an intact microbiota in females cancelled this male outbreeding strategy. As a consequence, the microbiota, when intact, decreased the fitness of the mating couple. Furthermore, we showed that female sexual signaling (cuticular hydrocarbons), with regards to kin recognition, significantly interacts with microbiota. Interestingly, the interaction is significant for hydrocarbons expressed by both sexes, but not for female-specific compounds. Taken together, our results suggest that microbiota can influence kin recognition by disfavoring male outbreeding strategies, likely by inhibiting key olfactory sexual signaling. This represents the first evidence of a host outbreeding strategy counteracted by their microbiota.

Highlights

The host microbiota is increasingly being shown to have important effects on host developmental, physiological, behavioral, and evolutionary processes
Female propensity to mate with unrelated males decreased when unrelated males developed on the same diet as the female compared to unrelated males that developed on a different diet (Tukey HSD, p = 0.026)
We found the major criterion determining female propensity to mate is the relatedness of the male they mate with, with mating being less probable with unrelated males compared to related ones

Summary

Introduction

The host microbiota is increasingly being shown to have important effects on host developmental, physiological, behavioral, and evolutionary processes. Some studies have shown that both wild and laboratory-reared females prefer to mate with related males over unrelated ones (Loyau et al, 2012; Robinson et al, 2012), with inbred flies preferring to mate with individuals reared on the same diet (Sharon et al, 2010; Najarro et al, 2015) As this effect disappears when the diet is supplemented with antibiotics, it has been suggested that these preferences in mate choice are mediated by the commensal gut microbiota (Sharon et al, 2010; but see Leftwich et al, 2017)

Methods

Results

Conclusion