Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

Abstract

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labour however is vulnerable to genetic elements that favour the development of their carriers into queens. Several factors, such as intra-colonial relatedness, can modulate the spread of such caste-biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modelling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between non-hybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard-wired caste determination. Overall, our results may help understand the repeated evolution towards remarkable reproductive systems (e.g. social hybridogenesis) observed in many ant species.