Loss of phenotypic plasticity generates genotype-caste association in harvester ants

Caste differentiation and reproductive division of labor are the hallmarks of insect societies [1]. In ants and other social Hymenoptera, development of female larvae into queens or workers generally results from environmentally induced differences in gene expression 2, 3 and 4. However, several cases in which certain gene combinations may determine reproductive status have been described in bees [5] and ants 6, 7, 8 and 9. We investigated experimentally whether genotype directly influences caste determination in two populations of Pogonomyrmex harvester ants in which genotype-caste associations have been observed. Each population contains two genetic lineages [10]. Queens are polyandrous 11 and 12 and mate with males of both lineages 6 and 7, but in mature colonies, over 95% of daughter queens have a pure-lineage genome, whereas all workers are of F1 interlineage ancestry 6, 7 and 8. We found that this pattern is maintained throughout the colony life cycle, even when only a single caste is being produced. Through controlled crosses, we demonstrate that pure-lineage eggs fail to develop into workers even when interlineage brood are not present. Thus, environmental caste determination in these individuals appears to have been lost in favor of a hardwired genetic mechanism. Our results reveal that genetic control of reproductive fate can persist without loss of the eusocial caste structure