Transmission mode shapes host specialization of the phyllosphere microbiome

The collection of microorganisms inhabiting aboveground plant tissue, termed the phyllosphere microbiome, is shaped by both microbial dispersal and host filtering effects. Because plants often occur in multispecies assemblages, microbiome diversity is likely shaped by plant community composition through microbial transmission between conspecific (same species) and heterospecific (different species) host plants. Although rarely examined, the relative incidence of con-versus heterospecific transmission should impact microbiome-level specialization. Using four species of plants we experimentally tested this idea by passaging an initially diverse microbial community either between conspecific or heterospecific plants in the greenhouse. While conspecific transmission lines exhibited persistent host effects, these effects decreased in the heterospecific transmission lines, suggesting a shift towards more generalist microbiomes. Similarly, when microbiomes were transplanted onto a set of novel host plant species, host effects were weaker for these heterospecific lines than the conspecific lines. Finally, microbiomes conspecifically passaged on tomato plants were found to outcompete those passaged on either bean or pepper when co-inoculated onto tomato hosts, suggesting microbiome-level host specialization under conspecific transmission. Overall, we find that both transmission mode and host association history shape microbiome diversity, that repeated conspecific transmission results in microbiome specialization, and that repeated heterospecific transmission can drive microbiomes to develop generalist characteristics.