Milk bioactives may manipulate microbes to mediate parent-offspring conflict

Abstract

Among mammals, milk constituents directly influence the ecology of the infant's commensal microbiota. The immunological and nutritional impacts of breast milk and microbiota are increasingly well understood; less clear are the consequences for infant behavior. Here, we propose that interactions among bioactives in mother's milk and microbes in the infant gut contribute to infant behavioral phenotype and, in part, have the potential to mediate parent-offspring conflict. We hypothesize that infant behavior likely varies as a function of their mother's milk composition interacting with the infant's neurobiology directly and indirectly through the commensal gut bacteria. In this article, we will explore our hypothesis of a milk-microbiota-brain-behavior dynamic in the context of the coevolution between human milk oligosaccharides, bacteria, the gut-brain axis and behavior. Integrating established features of these systems allows us to generate novel hypotheses to motivate future research and consider potential implications of current and emerging clinical treatments.

Keywords: commensal bacteria; human milk oligosaccharides; infant development; lactation; maternal investment; microbiota.

Figure 1.

Conceptual model of bioactives in milk mediating maternal-offspring conflict and coordination. Bioactives in milk affect gut microbiota in the infant, impacting the development of neurobiology and subsequently behavior.

Figure 2.

The gut–brain axis pathways by which gut microbiota can affect neurobiology and subsequently behavior. Bacteria (blue rods and olive green circles) can produce neurotransmitters (yellow circles) or extract them from the gut lumen. Neurotransmitters can then interact with nerve cells of the vagus nerve or be released into portal circulation and possibly interact with other nerve cells. Microbiota can induce immune cell (red circles) activation or release hormones (purple circles). Bacterial species can also competitively inhibit other species, effectively selecting the metabolites able to be produced in the gut.

Figure 3.

The relationship between constraints and less costly phenotypes. The intensity of constraints (red indicates severe; blue indicates relaxed) on the mother–infant dyad affects the definition of a ‘less costly’ phenotype from a maternal resource perspective. Under situations of mild constraints (A and D), less costly phenotypes will prioritize growth or behavior because resources are not available to prioritize both. Under severe constraints (C), less costly phenotypes will be delayed in both growth and behavior. Under relaxed constraints (B), resources can be allocated to behavior and growth.