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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. [ABSTRACT FROM AUTHOR]

A remarkable social polymorphism is controlled by a single Mendelian factor in the fire ant Solenopsis invicta. A genomic element marked by the gene Gp-9 determines whether workers tolerate one or many fertile queens in their colony. Gp-9 was recently shown to be part of a supergene with two nonrecombining variants, SB and Sb. SB/ SB and SB/Sb queens differ in how they initiate new colonies, and in many physiological traits, for example odour and maturation rate. To understand how a single genetic element can affect all these traits, we used a microarray to compare gene expression patterns between SB/ SB and SB/Sb queens of three different age classes: 1-day-old unmated queens, 11-day-old unmated queens and mated, fully reproductive queens collected from mature field colonies. The number of genes that were differentially expressed between SB/ SB and SB/Sb queens of the same age class was smallest in 1-day-old queens, maximal in 11-day-old queens and intermediate in reproductive queens. Gene ontology analysis showed that SB/ SB queens upregulate reproductive genes faster than SB/Sb queens. For all age classes, genes inside the supergene were overrepresented among the differentially expressed genes. Consistent with the hypothesized greater number of transposons in the Sb supergene, 13 transposon genes were upregulated in SB/Sb queens. Viral genes were also upregulated in SB/Sb mature queens, consistent with the known greater parasite load in colonies headed by SB/Sb queens compared with colonies headed by SB/ SB queens. Eighteen differentially expressed genes between reproductive queens were involved in chemical signalling. Our results suggest that many genes in the supergene are involved in regulating social organization and queen phenotypes in fire ants. [ABSTRACT FROM AUTHOR]