Intragenomic conflict underlies extreme phenotypic plasticity in queen-worker caste determination in honey bees (Apis mellifera)

Abstract

Caste determination of honey bees (Apis mellifera) is a prime example of developmental plasticity, where differences in larval diet will result in identical genotypes yielding either long-lived, reproductive queens or short-lived, facultatively sterile workers. Beyond environmental factors, intragenomic conflict between genes inherited from the mother (matrigenes) versus the father (patrigenes) is also hypothesized to generate this plasticity. In honey bees, the Kinship Theory of Intragenomic Conflict predicts selection on patrigenes to enhance traits that result in fitness gained through reproduction, and thus patrigenes should favor the queen caste fate. Here, we conducted allele-specific transcriptome analyses on queen-destined larvae (QL) and worker-destined larvae (WL) at 192 hours post-fertilization (hpf), a critical stage for caste determination. Our findings reveal hundreds of genes with parent-of-origin effects (POEs), with significant patrigene-biased transcription in QL. Genes with POEs in honey bees resemble imprinted genes in other taxa in terms of genomic clustering, recombination rate, intron length and CpG density, and a subset are maintained from 24hpf eggs. Previous studies demonstrated that DNA methylation, the canonical regulatory mechanism underlying transcriptional POEs in placental mammals, angiosperms, and some insects, is not operating in honey bees or other social insects. We use allele-specific ChIP-seq analyses to demonstrate that POEs on caste-specific histone post-translational modification (HPTM) profiles of H3K27me3, H3K4me3 and H3K27ac are associated with POEs on transcription. Together, these findings suggest that parent-of-origin intragenomic conflicts may contribute broadly to phenotypic plasticity and may be associated with HPTMs, suggesting a “non-canonical” genomic imprinting-like system in social insects.