Living in nests is an almost universal feature of eusocial animals. In some aphids, however, sterile soldier castes have evolved in open colonies without a nest. To clarify the factors promoting the evolution of eusociality in these colonies, we used newly developed microsatellite markers to compare the kin structure of the open colonies of two aphid species on bamboo: the non-eusocial colonies of Astegopteryx bambucifoliae and the eusocial colonies of Pseudoregma alexanderi on Dendrocalamus latiflorus.

Our samples, from over 1000 hectares, contained 99 clones of A. bambucifoliae and 19 of P. alexanderi. Clonal mixing occurred in both species: average pairwise relatedness within a colony was 0.54 in A. bambucifoliae and 0.71 in P. alexanderi. Each clone of A. bambucifoliae occurred in a unique location, whereas those of P. alexanderi occurred in multiple locations and more than 90% of individuals came from just four clones. There was significant genetic variation among different colonies in the same clump (stem-cluster) in A. bambucifoliae but not in P. alexanderi, indicating that P. alexanderi colonies in a single clump are genetically homogenised, functioning as a large colony. In P. alexanderi, the proportion of sterile soldiers to normal first-instar nymphs was significantly different across the four clones.

Our results indicate that the lack of input of migrants from the primary host and feeding on a large, stable host plant are important ecological factors that might favour the evolution of eusociality, enabling the production of genetically homogenised, large, and long-lived colonies. After eusociality evolves on the secondary host, the optimal strategy of soldier production might vary between different clones.