Eusocial evolution without a nest: kin structure of social aphids forming open colonies on bamboo

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: the non-eusocial Astegopteryx bambucifoliae and the eusocial Pseudoregma alexanderi. Our samples, from over 1,000 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 homogenized, 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, combined with feeding on a large, stable host plant, are the key ecological factors that favour the evolution of eusociality, enabling the production of genetically homogenised, large, and long-lived colonies. After eusociality evolves, the optimal strategy of soldier production might vary between different clones. Significance Statement Nest-living has often been considered to be a necessary condition for the evolution of eusociality. In a small number of aphid species, however, sterile soldier castes have evolved in open colonies without a nest. To understand why these aphids are unique, we examined the kin structure and genetic relatedness of individuals within open colonies of a eusocial and a non-eusocial aphid species. We found that clonal mixing occurred in both species, but the colonies of the eusocial species on bamboo are more genetically homogenized, functioning as a large colony. Our results suggest that ecological conditions that promote genetically homogenized, large and long-lived colonies are critical for the evolution of eusociality in these aphids. We propose that the open colonies of social aphids provide an ideal model system in which to study the evolution of altruism.