Strong support for the theory of kin selection can come from predicting outcomes under circumstances of within-family conflict. Genes inherited from mothers (matrigenes) and fathers (patrigenes) usually work harmoniously in the offspring. However, kin selection theory predicts these genes may be in conflict over interactions among relatives in which they are unequally represented (half-siblings). In honey bees, patrigenes are predicted to favor daughters that lay eggs themselves rather than remaining sterile and rearing their half-sisters' offspring. We tested this prediction, using crosses of distinct genetic stocks. Workers displayed the reproductive characteristics of their paternal genomes, patrigene expression was higher in reproductive tissues, and this patrigene bias increased in reproductive workers. These results provide strong empirical support for kin selection theory.

Abstract

Sexual reproduction brings genes from two parents (matrigenes and patrigenes) together into one individual. These genes, despite being unrelated, should show nearly perfect cooperation because each gains equally through the production of offspring. However, an individual’s matrigenes and patrigenes can have different probabilities of being present in other relatives, so kin selection could act on them differently. Such intragenomic conflict could be implemented by partial or complete silencing (imprinting) of an allele by one of the parents. Evidence supporting this theory is seen in offspring–mother interactions, with patrigenes favoring acquisition of more of the mother's resources if some of the costs fall on half-siblings who do not share the patrigene. The kinship theory of intragenomic conflict is little tested in other contexts, but it predicts that matrigene–patrigene conflict may be rife in social insects. We tested the hypothesis that honey bee worker reproduction is promoted more by patrigenes than matrigenes by comparing across nine reciprocal crosses of two distinct genetic stocks. As predicted, hybrid workers show reproductive trait characteristics of their paternal stock, (indicating enhanced activity of the patrigenes on these traits), greater patrigenic than matrigenic expression, and significantly increased patrigenic-biased expression in reproductive workers. These results support both the general prediction that matrigene–patrigene conflict occurs in social insects and the specific prediction that honey bee worker reproduction is driven more by patrigenes. The success of these predictions suggests that intragenomic conflict may occur in many contexts where matrigenes and patrigenes have different relatednesses to affected kin.