Integrative Genomics Reveals the Genetics and Evolution of the Honey Bee's Social Immune System

Citation

Harpur, B.A., Guarna, M.M., Huxter, E., Higo, H., Moon, K.M., Hoover, S.E., Ibrahim, A., Melathopoulos, A.P., Desai, S., Currie, R.W., Pernal, S.F., Foster, L.J., Zayed, A., Eyre-Walker, A. (2019). Integrative Genomics Reveals the Genetics and Evolution of the Honey Bee's Social Immune System, 11(3), 937-948. http://dx.doi.org/10.1093/gbe/evz018

Plain language summary

Social organisms live in multigenerational groups, often in large numbers. Although this arrangement increases the opportunity for the spread of disease, it also confers advantages for these organisms - through social immunity. This refers to behaviours that protect the group as a whole, from diseases and pests.

The honey bee is an excellent example of an organism that displays social immunity. Specifically, “nurse bees” can exhibit a trait known as “hygienic behaviour”. Hygienic bees detect infected, parasitized or dead larvae or pupae (immature bees) and remove them from the colony before the disease becomes infectious; previous research has shown this behaviour is effective in reducing pests and diseases in hives and is inherited from one generation to the next. As an emerging field of study, the evolutionary and genetic mechanisms behind social immunity are still unknown; the goal of this research was to integrate the study of genetics and social immunity.

To do this, we selectively bred two groups of bees that highly expressed hygienic behaviour and compared them to an unselected group that did not highly express this trait. From all three groups, we collected samples of larvae and analyzed their genome (complete DNA sequence) of each. By comparing the hygienic and unselected groups, we determined that 73 genes were associated with hygienic behaviour. Further analysis was performed referencing Gene Ontology, a global database containing information about the function of genes. Overall, genes associated with hygienic behaviour in honey bees were also found to be associated with brain development and odour perception in solitary insects. Our results suggest that genes influencing neurobiology and behaviour in solitary insects were shaped through evolution to give rise to social immunity traits that confer specific advantages to insects living in a social environment.

Abstract

© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. Social organisms combat pathogens through individual innate immune responses or through social immunity behaviors among individuals that limit pathogen transmissionwithin groups.Althoughwe have a relatively detailed understanding of the genetics and evolutionof the innateimmunesystemof animals,we knowlittle about socialimmunity.Addressing this knowledgegapis crucial for understanding how life-history traits influence immunity, and identifying if trade-offs exist between innate and social immunity. Hygienic behavior in theWestern honey bee, Apismellifera, provides an excellent model for investigating the genetics and evolution of socialimmunity in animals. This heritable, colony-level behavior is performed by nurse beeswhen they detect and remove infected or dead brood fromthe colony.We sequenced 125 haploid genomes fromtwo artificially selected highly hygienic populations and a baseline unselectedpopulation.Genomic contrastsallowedus toidentify aminimumof73genes tentatively associatedwithhygienic behavior. Many genes were within previously discovered QTLs associated with hygienic behavior and were predictive of hygienic behavior within the unselected population. These genes were often involved in neuronal development and sensory perception in solitary insects.We found that genes associatedwith hygienic behavior have evidence of positive selectionwithin honey bees (Apis), supporting the hypothesis that social immunity contributes to fitness. Our results indicate that genes influencing developmental neurobiology andbehavior insolitary insectsmayhavebeenco-optedtogive rise toa novel andadaptive social immunephenotype in honey bees.

Publication date

2019-01-01