A depauperate immune repertoire precedes evolution of sociality in bees

Abstract

BackgroundSociality has many rewards, but can also be dangerous, as high population density and low genetic diversity, common in social insects, is ideal for parasite transmission. Despite this risk, honeybees and other sequenced social insects have far fewer canonical immune genes relative to solitary insects. Social protection from infection, including behavioral responses, may explain this depauperate immune repertoire. Here, based on full genome sequences, we describe the immune repertoire of two ecologically and commercially important bumblebee species that diverged approximately 18 million years ago, the North American Bombus impatiens and European Bombus terrestris.ResultsWe find that the immune systems of these bumblebees, two species of honeybee, and a solitary leafcutting bee, are strikingly similar. Transcriptional assays confirm the expression of many of these genes in an immunological context and more strongly in young queens than males, affirming Bateman’s principle of greater investment in female immunity. We find evidence of positive selection in genes encoding antiviral responses, components of the Toll and JAK/STAT pathways, and serine protease inhibitors in both social and solitary bees. Finally, we detect many genes across pathways that differ in selection between bumblebees and honeybees, or between the social and solitary clades.ConclusionsThe similarity in immune complement across a gradient of sociality suggests that a reduced immune repertoire predates the evolution of sociality in bees. The differences in selection on immune genes likely reflect divergent pressures exerted by parasites across social contexts.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0628-y) contains supplementary material, which is available to authorized users.

Reduced cellular immune response in social insect lineages

“…However, new evidence suggests that the reduced repertoire of immune genes in A. mellifera precedes the evolution of sociality in bees [24], a complexity not yet well accounted for. Nonetheless, the accelerated rates of evolution in immune rsbl.royalsocietypublishing.org Biol.…”

Innate expression of antimicrobial peptides does not explain genotypic diversity in resistance to fungal brood parasites in the honey bee

“…There is accumulating evidence that bees (and possibly Hymenoptera) have a reduced number of immune genes in comparison to other insects (Evans et al 2006;Barribeau et al 2015), but honey bees are nonetheless subject to a broad range of microparasites against which individual immune responses are effective (Morse and Flottum 1997) and which will therefore play an important role in reducing levels of parasites within the colony. The antimicrobial peptide (AMP) abaecin is a key honey bee immune effector involved in the response to infection by multiple parasites (Casteels et al 1990;Evans and Pettis 2005;Evans et al 2006) and has been shown to have significant heritable variation in its expression (Decanini et al 2007).…”

Transitional Complexity of Social Insect Immunity

“…Therefore, honey bees would not rely on innate immunity as much as solitary insects. However, more recent comparative genomic studies of multiple insect genomes across different levels of social organization, indicated that eusociality by itself does not appear to affect the number of immunity-related genes in hymenopteran ants and bees (Wurm and Keller, 2010;Smith et al, 2011;Simola et al, 2013;Roux et al, 2014;Barribeau et al, 2015;Grozinger and Robinson, 2015;Kapheim et al, 2015;Sadd et al, 2015) or isopteran termites (Terrapon et al, 2014;Korb et al, 2015), challenging the previous hypothesis of eusociality causing relaxed selection on innate immunity. While these further analyses have supplied evidence that eusociality by itself is not associated with the reduction in immune-gene counts, the old claim is still being propagated in the recent literature (e.g., Nish and Medzhitov, 2011;Gadau et al, 2012;Mattila et al, 2012;Schöning et al, 2012;Evison et al, 2013;Meunier, 2015).…”

“…Therefore, to resolve the question of whether a transition to a eusocial lifestyle affects the number of immunity-related genes or not, future studies should focus on adopting multi-levelomics comparisons. With the application of this method, it would be possible to properly investigate whether transition to eusociality brings about a reduction in immunity-related genes in bees (Wurm and Keller, 2010;Barribeau et al, 2015;Kapheim et al, 2015). In particular, Barribeau et al compared immunityrelated genes from advanced eusocial, intermediate eusocial, and solitary bees (Libbrecht and Keller, 2015), and found comparable numbers of immunity-related genes between the bees regardless of the level of their sociality .…”

“…We then discuss the up-and-coming field of microbe-derived immunity and emphasize that gene-and microbe-level immunity should be investigated in parallel when studying the transitional gradients from a solitary to eusocial lifestyle, in order to form an integrated understanding of immunity as a whole. Finally, we recommend that (1) standardized approaches should be adopted for gene annotation and sequencing, (2) comparison of immunity should include multiple species representing different levels of sociality within a phylogenetic context, if possible, to capture transitional changes (e.g., Barribeau et al, 2015;Kapheim et al, 2015), and (3) functional experiments should be carried out to improve our understanding of differentially regulated genes of unknown function.…”