Evolutionary consequences of microbiomes for hosts: impacts on host fitness, traits, and heritability

Abstract

An organism's phenotypes and fitness often depend on the interactive effects of its genome (Gh⁢o⁢s⁢t), microbiome (Gm⁢i⁢c⁢r⁢o⁢b⁢e), and environment (E). These G × G, G × E, and G × G × E effects fundamentally shape host-microbiome (co)evolution and may be widespread, but are rarely compared within a single experiment. We collected and cultured L⁢e⁢m⁢n⁢am⁢i⁢n⁢o⁢r (duckweed) and its associated microbiome from 10 sites across an urban-to-rural ecotone. We factorially manipulated host genotype and microbiome in two environments (low and high zinc, an urban aquatic stressor) in an experiment with 200 treatments: 10 host genotypes × 10 microbiomes × 2 environments. Host genotype explained the most variation in L.m⁢i⁢n⁢o⁢r fitness and traits, while microbiome effects often depended on host genotype (G × G). Microbiome composition predicted G × G effects: when compared in more similar microbiomes, duckweed genotypes had more similar effects on traits. Further, host fitness increased and microbes grew faster when applied microbiomes more closely matched the host's field microbiome, suggesting some local adaptation between hosts and microbiota. Finally, selection on and heritability of host traits shifted across microbiomes and zinc exposure. Thus, we found that microbiomes impact host fitness, trait expression, and heritability, with implications for host-microbiome evolution and microbiome breeding.