Dataset Information

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.

SUBMITTER: Harpur BA

PROVIDER: S-EPMC6447389 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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

Harpur Brock A BA Guarna Maria Marta MM Huxter Elizabeth E Higo Heather H Moon Kyung-Mee KM Hoover Shelley E SE Ibrahim Abdullah A Melathopoulos Andony P AP Desai Suresh S Currie Robert W RW Pernal Stephen F SF Foster Leonard J LJ Zayed Amro A

Genome biology and evolution 20190301 3

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 s ...[more]

PMID: 30768172

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Project description:Background Honey bee gut microbiota transmitted via social interactions are beneficial to the host health. Although the microbial community is relatively stable, individual variations and high strain-level diversity have been detected across honey bees. Although the bee gut microbiota structure is influenced by environmental factors, the heritability of the gut members and the contribution of the host genetics remains elusive. Considering bees within a colony are not readily genetically identical due to the polyandry of the queen, we hypothesize that the microbiota structure can be shaped by host genetics. Results We used shotgun metagenomics to simultaneously profile the microbiota and host genotypes of bees from hives of four different subspecies. Gut composition is more distant between genetically different bees at both phylotype- and “sequence-discrete population” levels. We then performed a successive passaging experiment within colonies of hybrid bees generated by artificial insemination, which revealed that the microbial composition dramatically shifts across batches of bees during the social transmission. Specifically, different strains from the phylotype of Snodgrassella alvi are preferentially selected by genetically varied hosts, and strains from different hosts show a remarkably biased distribution of single-nucleotide polymorphism in the Type IV pili loci. Genome-wide association analysis identified that the relative abundance of a cluster of Bifidobacterium strains is associated with the host glutamate receptor gene specifically expressed in the bee brain. Finally, mono-colonization of Bifidobacterium with a specific polysaccharide utilization locus impacts the alternative splicing of the gluR-B gene, which is associated with an increased GABA level in the brain. Conclusions Our results indicated that host genetics influence the bee gut composition and suggest a gut-brain connection implicated in the gut bacterial strain preference. Honey bees have been used extensively as a model organism for social behaviors, genetics, and the gut microbiome. Further identification of host genetic function as a shaping force of microbial structure will advance our understanding of the host-microbe interactions. Video abstract Supplementary Information The online version contains supplementary material available at 10.1186/s40168-021-01174-y.

Dataset Information

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

Publications

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

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