Finer-Scale Phylosymbiosis: Insights from Insect Viromes

Abstract

Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern whereby the ecological relatedness (e.g., beta diversity relationships) of host-associated microbial communities parallels the phylogeny of the host species. Representing the most abundant biological entities on the planet and common members of the animal-associated microbiome, viruses can be influential members of host-associated microbial communities that may recapitulate, reinforce, or ablate phylosymbiosis. Here we sequence the metagenomes of purified viral communities from three different parasitic wasp <i>Nasonia</i> species, one cytonuclear introgression line of <i>Nasonia</i>, and the flour moth outgroup Ephestia kuehniella. Results demonstrate complete phylosymbiosis between the viral metagenome and insect phylogeny. Across all <i>Nasonia</i> contigs, 69% of the genes in the viral metagenomes are either new to the databases or uncharacterized, yet over 99% of the contigs have at least one gene with similarity to a known sequence. The core <i>Nasonia</i> virome spans 21% of the total contigs, and the majority of that core is likely derived from induced prophages residing in the genomes of common <i>Nasonia</i>-associated bacterial genera: <i>Proteus</i>, <i>Providencia</i>, and <i>Morganella</i>. We also assemble the first complete viral particle genomes from <i>Nasonia</i>-associated gut bacteria. Taken together, results reveal the first complete evidence for phylosymbiosis in viral metagenomes, new genome sequences of viral particles from <i>Nasonia</i>-associated gut bacteria, and a large set of novel or uncharacterized genes in the <i>Nasonia</i> virome. This work suggests that phylosymbiosis at the host-microbiome level will likely extend to the host-virome level in other systems as well. <b>IMPORTANCE</b> Viruses are the most abundant biological entity on the planet and interact with microbial communities with which they associate. The virome of animals is often dominated by bacterial viruses, known as bacteriophages or phages, which can (re)structure bacterial communities potentially vital to the animal host. Beta diversity relationships of animal-associated bacterial communities in laboratory and wild populations frequently parallel animal phylogenetic relationships, a pattern termed phylosymbiosis. However, little is known about whether viral communities also exhibit this eco-evolutionary pattern. Metagenomics of purified viruses from recently diverged species of <i>Nasonia</i> parasitoid wasps reared in the lab indicates for the first time that the community relationships of the virome can also exhibit complete phylosymbiosis. Therefore, viruses, particularly bacteriophages here, may also be influenced by animal evolutionary changes either directly or indirectly through the tripartite interactions among hosts, bacteria, and phage communities. Moreover, we report several new bacteriophage genomes from the common gut bacteria in <i>Nasonia</i>.