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 labor, however, is vulnerable to genetic elements that favor the development of their carriers into queens. Several factors, such as intracolonial 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 modeling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between nonhybrid 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 toward remarkable reproductive systems (e.g., social hybridogenesis) observed in several ant species.