Maternal transmission as a microbial symbiont sieve, and the absence of lactation in male mammals

Abstract

Gut microbiomes of humans carry a complex symbiotic assemblage of microorganisms. As in all mammals, the special mode of feeding newborn infants through milk from the mammary gland enhances the opportunity for vertical transmission of the milk microbiome from parents to the gut microbiome of offspring. This has potential benefits, but it also brings with it some hazards for the host. Here we use mathematical and numerical models to demonstrate that vertical transmission from both parents would allow host populations to be invaded by microbiome elements that are deleterious. In contrast, vertical transmission, when restricted to one parent, acts as a sieve preventing the spread of such elements. We show that deleterious symbionts generate selection for uniparental transmission in host populations, and that this selective advantage is maintained in the presence of moderate horizontal transmission. Some vertical transmission from mother to infant is bound to happen in placental mammals. This paper therefore puts forward the hypothesis that the asymmetry between females and males, together with the hazards that come with biparental transmission of the milk microbiome, generate selection against male lactation in humans, and in mammals in general.