Advanced societies owe their success to an efficient division of labour that, in some social insects, is based on specialized worker phenotypes. The system of caste determination in such species is therefore critical. Here, we examine in a leaf-cutting ant (Acromyrmex echinatior) how a recently discovered genetic influence on caste determination interacts with the social environment. By removing most of one phenotype (large workers; LW) from test colonies, we increased the stimulus for larvae to develop into this caste, while for control colonies we removed a representative sample of all workers so that the stimulus was unchanged. We established the relative tendencies of genotypes to develop into LW by genotyping workers before and after the manipulation. In the control colonies, genotypes were similarly represented in the large worker caste before and after worker removal. In the test colonies, however, this relationship was significantly weaker, demonstrating that the change in environmental stimuli had altered the caste propensity of at least some genotypes. The results indicate that the genetic influence on worker caste determination acts via genotypes differing in their response thresholds to environmental cues and can be conceptualized as a set of overlapping reaction norms. A plastic genetic influence on division of labour has thus evolved convergently in two distantly related polyandrous taxa, the leaf-cutting ants and the honeybees, suggesting that it may be a common, potentially adaptive, property of complex, genetically diverse societies.