Kathrin Näpflin

A depauperate immune repertoire precedes evolution of sociality in bees

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.

Immune response and gut microbial community structure in bumblebees after microbiota transplants.

Microbial communities are a key component of host health. As the microbiota is initially ‘foreign’ to a host, the hosts immune system should respond to its acquisition. Such variation in the response should relate not only to host genetic background, but also to differences in the beneficial properties of the microbiota. However, little is known about such interactions. Here, we investigate the gut microbiota of the bumblebee, Bombus terrestris, which has a protective function against the bees natural trypanosome gut parasite, Crithidia bombi. We transplanted ‘resistant’ and ‘susceptible’ microbiota into ‘resistant’ and ‘susceptible’ host backgrounds, and studied the activity of the host immune system. We found that bees from different resistance backgrounds receiving a microbiota differed in aspects of their immune response. At the same time, the elicited immune response also depended on the received microbiotas resistance phenotype. Furthermore, the microbial community composition differed between microbiota resistance phenotypes (resistant versus susceptible). Our results underline the complex feedback between the hosts ability to potentially exert selection on the establishment of a microbial community and the influence of the microbial community on the host immune response in turn.

High Gut Microbiota Diversity Provides Lower Resistance against Infection by an Intestinal Parasite in Bumblebees

The microbiome, especially the gut flora, is known to affect the interaction between parasites and their hosts. In this context, a parasitic infection can be viewed as an invasion into the preexisting microbial ecological community. Hence, in addition to the intrinsic defense mechanisms of the host itself, infection success depends on the colonization resistance of the microbiota. In the bumblebee Bombus terrestris, the microbiota provides resistance to the intestinal parasite Crithidia bombi, yet which properties actually provide protection remains largely unknown. Here, we show that the community structure of the gut microbiota—in terms of bacterial operational taxonomic units (OTUs) of 16S ribosomal RNA gene sequences—before parasite exposure can be informative of the eventual infection outcome. Specifically, higher microbiota OTU diversity is associated with less resistance. However, the microbial community structure does not differ between infected and noninfected individuals or between infected individuals of varying susceptibility. This suggests that parasite infection success depends on the microbiota composition but that subsequent changes occur, although the exact alteration that occurs remains elusive. In fact, the bumblebee microbiota is surprisingly unaffected by parasite exposure and infection. Rather, the microbiota-host interaction before parasite exposure seems to be a key mechanism regulating resistance to infection.