Temporal division of labor in an aphid social system

Temporal division of labor, or age polyethism, in which altruistic caste individuals change their tasks with aging, is widely found in bees and ants (Hymenoptera) and also in other social insects. Here we report the discovery of elaborate age polyethism in a social aphid (Hemiptera). Tuberaphis styraci is a gall-forming aphid in which monomorphic first instar nymphs differentiate into normal nymphs and soldiers upon second instar molt. Soldiers neither grow nor reproduce but perform gall cleaning and colony defense. Using an artificial diet rearing system, we collected age-defined groups of soldiers and monitored their social behaviors. We observed that young soldiers tend to clean whereas old soldiers preferentially attack, thereby verifying age-dependent task switching from housekeeping to defense. Strategic sampling, age estimation and behavioral observation of soldiers from natural galls revealed that (1) young cleaning soldiers tend to inhabit upper gall regions with adult insects, (2) old attacking soldiers tend to be distributed in lower gall regions, particularly around the gall openings, and (3) the gall structure is linked to intra-nest movement, aging and task switching of soldiers in an adaptive manner. These results highlight an evolutionary parallelism comparable to the sophisticated temporal division of labor observed in honeybee colonies.