Beyond conflict: Kinship theory of intragenomic conflict predicts individual variation in altruistic behaviour

Abstract

Behavioural variation is essential for animals to adapt to different social and environmental conditions. The Kinship Theory of Intragenomic Conflict (KTIC) predicts that parent‐specific alleles can support different behavioural strategies to maximize allele fitness. Previous studies, including in honey bees (Apis mellifera), supported predictions of the KTIC for parent‐specific alleles to promote selfish behaviour. Here, we test the KTIC prediction that for altruism‐promoting genes (i.e. those that promote behaviours that support the reproductive fitness of kin), the allele with the higher altruism optimum should be selected to be expressed while the other is silenced. In honey bee colonies, workers act altruistically when tending to the queen by performing a ‘retinue’ behaviour, distributing the queen's mandibular pheromone (QMP) throughout the hive. Workers exposed to QMP do not activate their ovaries, ensuring they care for the queen's brood instead of competing to lay unfertilized eggs. Due to the haplodiploid genetics of honey bees, the KTIC predicts that response to QMP is favoured by the maternal genome. We report evidence for parent‐of‐origin effects on the retinue response behaviour, ovarian development and gene expression in brains of worker honey bees exposed to QMP, consistent with the KTIC. Additionally, we show enrichment for genes with parent‐of‐origin expression bias within gene regulatory networks associated with variation in bees' response to QMP. Our study demonstrates that intragenomic conflict can shape diverse social behaviours and influence expression patterns of single genes as well as gene networks.