Trematodes form clonal colonies in their first intermediate host. Individuals are, depending on species, rediae or sporocysts (which asexually reproduce) and cercariae (which develop within rediae or sporocysts and infect the next host). Some species use a division of labour within colonies, with 2 distinct redial morphs: small rediae (non-reproducing) and large rediae (individuals which produce cercariae). The theory of optimal caste ratio predicts that the ratio of caste members (small to large rediae) responds to environmental variability. This was tested in Philophthalmus sp. colonies exposed to host starvation and competition with the trematode, Maritrema novaezealandensis. Philophthalmus sp. infected snails, with and without M. novaezealandensis, were subjected to food treatments. Reproductive output, number of rediae, and the ratio of small to large rediae were compared among treatments. Philophthalmus sp. colonies responded to host starvation and competition; reproductive output was higher in well-fed snails of both infection types compared with snails in lower food treatments and well-fed, single infected snails compared with well-fed double infected snails. Furthermore, the caste ratio in Philophthalmus sp. colonies was altered in response to competition. This is the first study showing caste ratio responses to environmental pressures in trematodes with a division of labour.