Phylosymbiosis and the hologenome in fungus-gardening ants

Abstract

Hosts and their microbiomes can be extensively integrated so that they behave across evolutionary scales as a single unit or as a hologenome. Hosts and their associated microbiomes can potentially exhibit concordance among their respective phylogenetic histories, a phenomenon known as phylosymbiosis. The obligate symbiosis of fungus-gardening ants represents a complex symbiotic system as there are two macroscopic hosts that have associated microbiomes. Here we apply 16S rRNA gene analysis of microbiomes in combination with phylogenetic analysis of nuclear genes and SNPs (single nucleotide polymomorphisms) of hosts to determine the extent to which phylosymbiosis characterizes the coevolution among ant hosts, fungal symbionts and bacterial microbiomes of five species of fungus-gardening ants. The strongest evidence of phylosymbiosis (i.e., congruent topologies between host phylogenetics and microbiome structure) was found between ants and ant-associated microbiomes. While fungal phylogenies and microbiome dendrograms were correlated, these correlations were not topologically congruent. We conclude that phylosymbiosis is present between the ant hosts and their ant-associated microbiome and this would be the strongest evidence of the hologenome concept within the attine symbiosis.