Using quantitative genetics to reveal structure-function relationships in host-microbe systems

Background/Question/Methods:  Understanding the relationship between microbial community structure and ecosystem function is challenging because of the extraordinary diversity of most microbial communities. This understanding is especially challenging for microbial communities associated with hosts, because host-microbe system-level traits arise not only through interactions that microbes have with each other and the environment, but also potentially through their interactions with hosts. We argue that progress in determining structure-function relationships in host-microbe systems requires a novel conceptualization that addresses the following: the degree to which these system-level traits are heritable and linked to fitness at various levels, how this heritability is influenced by genetic variation in both host genomes and the microbiota, and how transmission dynamics of hosts and microbes influences the heritability of host-microbe system traits. This re-conceptualization builds upon the rich and well-developed field of quantitative genetics, but requires the development of new theoretical and empirical approaches to expand this foundational body of work to fully embrace the unique nature of host-microbe systems.

Results/Conclusions:  Applying a quantitative genetics framework to understanding structure-function relationships in host-microbe systems requires first that functional traits at the system-level be identified. Such traits would be the product of some combination of host and microbiota genetics interacting with the external environment, and for those traits evolving adaptively would be linked to fitness at the level of the host-microbe system. Total variation in such traits (V_T) can be partitioned into that explained by variation in host genetics (V_G), by variation in the microbiota (V_M), and by environmental variation (V_E). The quantities V_G / V_T and V_M / V_T are the proportions of total variation in a host-microbe trait that are explained by host genetic and microbiota variation, and together comprise an analog of “heritability” (h²) in traditional quantitative genetics. This conceptualization of host genetic and microbiota components of heritability (h²_G and h²_M) suggests that well developed quantitative genetic theory and empirical approaches can be extended to better model and quantify microbial structure-function relationships in host-microbe systems. A particularly promising approach is measuring the response of a system-level function to artificial selection in order to calculate heritability and identify co-evolving host genetic and microbiota contributions to adaptive system-level traits.