Immunity vs Sociality: Adaptive evolution tests suggest social lifestyle exerts greater selection pressures than host-pathogen coevolution in the bees

Abstract

Hosts and their parasites and pathogens are locked in antagonistic co-evolution. The genetic consequence of this can be seen in the rates of adaptive evolution in immunologically important loci in many taxa. As the risk of disease transmission increases we might also expect to see greater rates of adaptive evolution on genes of immune function. The evolution of sociality and its elaborations in insects represent enormous shift in disease transmission risk. Here, we examine whether sociality in the bees corresponds to changes in the rate of adaptive evolution in both classical canonical immune genes, and genes with putative immune functions identified from meta-analyses of honey-bee transcriptomic responses to infection. We find that measures of gene-wide adaptive evolution do not differ among canonical immune, non-canonical candidate immune, and background gene sets, but that branch-site adaptive evolution does increase with sociality regardless of gene category. Solitary species have greater rates of adaptive evolution in canonical immune genes than background genes, supporting the suggestion that social immune mechanisms may instead be the site of host-pathogen co-evolution in social species. We identify three genes with putative roles in immunity that warrant further attention (Vitel-logenin Vg, disks large 1 tumour suppressor, and the uncharacterised protein LOC100577972). There are more gene family changes after the origin of sociality across all gene classes, with contractions occur-ring after the elaboration of sociality to complex eusociality. There are few genes or functions under adaptive selection that appear to be shared outside of specific lineages, suggesting that evolution of the immune system may be specific to individual species and their pathogen interactions. SignificanceInfectious disease drives rapid evolution of immune genes, but infection risk should be much higher in social species. To examine whether greater sociality drives faster immune system evolution we compared the rate of immune gene evolution in solitary, social, and highly eusocial bees. To account for possible novel immune genes in bees, we analysed classical immune genes alongside candidate immune genes inferred from other studies. Surprisingly, we find that solitary bees have the highest rate of immune gene evolution relative to background genes but that sociality is associated with rapid evolution across the whole genome. These findings suggest that 1) accelerated immune gene evolution is not universal, 2) immune gene evolution is moderated by sociality in that solitary species invest more into immune gene change, and 3) that social genomes are highly dynamic, which may obscure evolution at immunological loci. The types of immune genes and functions appear mostly lineage-specific, regardless of sociality, suggesting individual evolutionary his-tories exert more selection pressure than general patterns of greater pathogen exposure introduced by social living.