Microbiome breeding: conceptual and practical issues

Microbiome breeding is a new artificial selection technique that seeks to change the genetic composition of microbiomes in order to benefit plant or animal hosts. Recent experimental and theoretical analyses have shown that microbiome breeding is possible whenever microbiome-encoded genetic factors affect host traits (e.g., health) and microbiomes are transmissible between hosts with sufficient fidelity, such as during natural microbiome transmission between individuals of social animals, or during experimental microbiome transplanting between plants. To address misunderstandings that stymie microbiome-breeding programs, we (i) clarify and visualize the corresponding elements of microbiome selection and standard selection; (ii) elucidate the eco-evolutionary processes underlying microbiome selection within a quantitative genetic framework to summarize practical guidelines that optimize microbiome breeding; and (iii) characterize the kinds of host species most amenable to microbiome breeding. Microbiome breeding is a new technique to produce microbiomes that benefit hosts through artificial selection shaping the genetic composition of microbiomes, independently of any selection shaping host genomes.Theory predicts that microbiome breeding is possible whenever microbiomes can be transmitted between hosts with sufficient fidelity; successful microbiome-breeding methods therefore optimize microbiome stability and transmissibility.Microbiome-encoded genetic factors that influence host traits (e.g., health) are transmitted between hosts with different fidelities, ranging along a transmission–fidelity continuum; modeling a transmission continuum of microbiome-encoded genetic factors requires novel approaches.Microbiome breeding improves host traits by leveraging transplantable, microbiome-encoded genetic effects, with applications in agriculture, medicine, and microbial engineering.