Cash-Ahmed, A. C. | bioRxiv Science

bioRxiv2024

Molecular analyses of individual variation in honey bee sociability

Individual variation in sociability is a central feature of every society. This includes honey bees, with some individuals well-connected and sociable, and others at the periphery of their colonys social network. However, the genetic and molecular bases of sociability are poorly understood. Trophallaxis - a behavior involving sharing liquid with nutritional and signaling properties - comprises a social interaction and a proxy for sociability in honey bee colonies: more sociable bees engage in more trophallaxis. Here we identify genetic and molecular mechanisms of trophallaxis-based sociability by combining genome sequencing, brain transcriptomics, and automated behavioral tracking. A genome-wide association study (GWAS) identified 18 single-nucleotide polymorphisms (SNPs) associated with variation in sociability. Several SNPs were localized to genes previously associated with sociability in other species, including in the context of human autism, suggesting shared molecular mechanisms of sociability. Variation in sociability also was linked to differential brain gene expression, particularly genes associated with neural signaling and development. Using comparative genomic and transcriptomic approaches, we also detected evidence for divergent mechanisms underpinning sociability across species, including those related to reward sensitivity and encounter probability. These results highlight both potential evolutionary conservation of the molecular roots of sociability and points of divergence.

genomics↗

bioRxiv2022

Evolution of decreased aggression in honey bees targeted brain cell gene regulatory networks

Understanding how genotypic variation results in phenotypic variation, a major challenge in biology, is especially difficult for collective behaviour because collective group phenotypes arise from complex interactions between group members1. Honeybees aggressively defend their colony from attacks with highly integrated collective behaviour in which different groups of bees play specific roles, giving rise to distinct colony-level differences in aggression. A previous genome-wide association study of a population of Africanized honeybees (Apis mellifera scutellata) from Puerto Rico that recently evolved decreased aggression identified hundreds of genes with single nucleotide polymorphisms (SNPs) that associated with colony-level variation in aggression2. Many of these SNPs also showed strong signals of selection for decreased aggression2,3, but their influence on brain function was unknown. Using brain single-cell (sc) transcriptomics and sc gene regulatory network analysis, we show here that variants of these genes give rise to genetic differences in transcription factor-target gene relationships. These differences involved the activity of several TFs, some that have been previously associated with aggression, like single stranded-binding protein c31A, and some that have been associated with tissue morphogenesis but not behaviour, like apontic. The activity of these and other TFs was located in specific brain cell populations related to olfaction and vision, the two sensory modalities that bees use in colony defence. They also implicate metabolism of serotonin, a neurochemical already known to influence honeybee aggression, but not from a genetic perspective. Surprisingly, genetic differences were more pronounced in the brains of forager bees than in similarly aged but more aggressive soldier bees, pointing to an evolutionary change in division of labour for colony defence. Our results demonstrate how group genetics can shape a collective phenotype by modulating individual brain gene regulatory network architecture.

genomics↗