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

Abstract

Social organisms combat pathogens through individual innate immune responses or through social immunity—behaviors among individuals that limit pathogen transmission within groups. Although we have a relatively detailed understanding of the genetics and evolution of the innate immune system of animals, we know little about social immunity. Addressing this knowledge gap is crucial for understanding how life-history traits influence immunity, and identifying if trade-offs exist between innate and social immunity. Hygienic behavior in the Western honey bee, Apis mellifera , provides an excellent model for investigating the genetics and evolution of social immunity in animals. This heritable, colony-level behavior is performed by nurse bees when they detect and remove infected or dead brood from the colony. We sequenced 125 haploid genomes from two artificially selected highly hygienic populations and a baseline unselected population. Genomic contrasts allowed us to identify a minimum of 73 genes tentatively associated with hygienic 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 associated with hygienic behavior have evidence of positive selection within honey bees ( Apis ), supporting the hypothesis that social immunity contributes to fitness. Our results indicate that genes influencing developmental neurobiology and behavior in solitary insects may have been co-opted to give rise to a novel and adaptive social immune phenotype in honey bees.

Honey Bee Survival Mechanisms Against the Parasite <em>Varroa destructor</em>: A Systematic Review of Phenotypic and Genomic Research Efforts

“…Indeed, some loci appear to be linked to more than one social immunity trait ( Figure 5). For instance, some of the SNPs from the HYG investigations of Harpur et al (2019) fall within the locus found by Tsuruda et al (2012) when investigating VSH. However, more often, studies did not report the same regions to be involved, whether they were investigating the same trait or not.…”

“…Wider QTL bars indicate that the QTL was identified in more than one study. Genomic studies included Arechavaleta-Velasco et al 2012, Bourgeois et al 2016, Behrens et al 2012, Lattorff et al 2016, Conlon et al 2018, Conlon et al 2019, Tsuruda et al 2012, Spötter et al 2012, Harpur et al 2019, Oxley et al 2010, and Spötter et al 2016). The details of the genes, traits, and references are presented in Table S1 to S4.…”

“…In addition to the intra-colonial level, the variation of traits between colonies in a given population is of great importance. In natural conditions, the high admixture of drones in drone congregation areas provides opportunity for mixing of bee genotypes (Harpur et al 2019;Baudry et al, 1998), and may facilitate the spread of resistance traits. In A. mellifera, drone brood is highly attractive to varroa mites (Le Conte et al, 1989).…”

Ultraconserved non-coding DNA within insect phyla

“…4). Dscam2 is implicated in axon guidance in Drosophila (Millard et al 2007) and in regulation of social immunity behavior in honeybees (reviewed by Cremer et al 2007;Harpur et al 2019). The EvoPrint scorecard ( fig.…”

“…5). The Drosophila Gsc homeodomain transcription factor is required for proper axon wiring during embryonic CNS development and has recently been linked to social immunity behavior in honeybees (reviewed by Cremer et al 2007;Harpur et al 2019). The Drosophila Cas Zn-finger transcription factor has been shown to be essential for neuroblast temporal identity decisions during neural lineage development (Baumgardt et al 2014;reviewed by Brody and Odenwald 2007).…”