Larger, more connected societies of ants have a higher prevalence of viruses.

The benefits of cooperative living for foraging, nesting, defence and buffering environmental challenges lead animals with the most highly social lifestyles to dominate many ecosystems. However, living in larger, more highly connected groups should also increase the risks of pathogen exposure and transmission. While over long timescales selective responses could buffer the impacts of potential higher pathogen prevalence, similar processes are unlikely over short timescales. The red fire ant Solenopsis invicta is ideal for measuring the effects of group size on pathogen prevalence because two types of society coexist in this species: smaller single-nest single-queen colonies that are highly aggressive to their neighbours and larger multiple-queen colonies that exchange resources with neighbouring nests. We compare the presence of viruses between these two colony types using metagenomic sequence classification of RNA-sequencing reads. We find that queens from multiple-queen colonies have 8.3-times higher viral load and 1.5-times higher viral diversity than queens from single-queen colonies. This finding characterizes a rarely considered cost of transitions to more highly social living. Furthermore, our results show that highly social invertebrates can harbour many viruses.

Recurring adaptive introgression of a supergene variant that determines social organization.

Introgression has been proposed as an essential source of adaptive genetic variation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. This barrier might be overcome in supergene regions, where suppressed recombination leads to joint inheritance across many loci. Here, we study the evolution of a large supergene region that determines a major social and ecological trait in Solenopsis fire ants: whether colonies have one queen or multiple queens. Using coalescent-based phylogenies built from the genomes of 365 haploid fire ant males, we show that the supergene variant responsible for multiple-queen colonies evolved in one species and repeatedly spread to other species through introgressive hybridization. This finding highlights how supergene architecture can enable a complex adaptive phenotype to recurrently permeate species boundaries.