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

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

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.

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