Intragenomic conflict over queen determination favours genomic imprinting in eusocial Hymenoptera

Abstract

Colonies of eusocial Hymenoptera, such as ants, bees and wasps, have long been recognized as candidates for the study of genomic imprinting on the grounds of evolutionary conflicts that arise from close interactions among colony members and relatedness asymmetry owing to haplodiploidy. Although a general kinship theory of genomic imprinting predicts its occurrence under various circumstances of the colony life cycle, new theoretical approaches are required to account for the specifics of real colonies based on recent advances in molecular-level understanding of ants and honeybees. Using a multivariate quantitative genetic model, we examined the potential impact of genomic imprinting on genes that determine the carrier female's propensity to develop into the queen caste. When queen overproduction owing to the increased propensity comes at a colony-level cost, the conflict between maternally and paternally inherited genes in polyandrous (queen multiple mating) colonies favours genomic imprinting. Moreover, we show that the genomic imprinting can occur even under monandry (queen single mating), once incorporating the costs differentially experienced by new males and new queens. Our model predicts the existence of imprinted 'genetic royal cheats' with patriline-specific expression in polyandrous colonies, and seems consistent with the paternal effect on queen determination in monandrous Argentine ants.