Summary:

Social living offers many benefits, but comes with a greater risk of infection, especially when the groups are genetically homogenous, as in some social insects. Surprisingly, the first social insect genome, the honeybee, revealed a reduced immune system. Honeybees, like many other highly social insects mate multiply, producing a genetically diverse and complex colony for parasites to invade. Bumblebees, however, mate singly thereby producing dense colonies of highly related sisters. The bumblebee Bombus terrestris is commonly infected with a trypanosome gut parasite Crithidia bombi. Different genotypes of bumblebees are susceptible to different clones of parasite, but the factors that produce this complex pattern of host-parasite matching remain elusive. We took a transcriptomic approach to understand how bumblebees respond to this parasite and whether host-parasite matching is driven by gene expression differences. We find exceptionally high variation in gene expression upon infection despite the low genetic diversity among sisters. This variation among individuals may be especially important in producing an immunologically diverse population, buffering the colony from parasite spread. We also find that different host genotypes down-regulate the same genes but up-regulate distinct suites of genes upon infection. This pattern suggests a core shared signal of infection, but a unique suite of up-regulated genes. We also find that clones of this parasite alter expression of their hosts differently. Highly infectious clones down regulate important immunological genes such as antimicrobial peptides but colonies differ in the scale of this effect. Host-parasite specificity may be generated by these specific patterns of expression. We discuss how parasites may manipulate host immune responses for their own gain and how variation among workers may contribute to the sustainability of highly related insect societies in a parasite rich world.