Genetic conflict and conditional altruism in social aphid colonies

Abstract

Although kin selection is central to the modern study of social evolution, recent studies of social species have revealed that no simple relationship exists between levels of kinship and sociality. The soldier-producing aphids are unique among highly social animals because, barring movement by aphids between colonies, they occur in clonal groups of genetically identical individuals. Potentially, clonality simplifies efforts to understand social evolution in aphids by obviating issues of intragroup conflict. However, we report here high levels of clonal mixing and conflict in an aphid society. The gall-dwelling colonies of a social aphid species (Pemphigus obesinymphae) are not pure clones, but are invaded by large numbers of aphids from other clones. Intruders behave and develop selfishly once they have invaded a colony of nonkin. They refrain from risky defensive behaviors and accelerate their own development into reproductive rather than defensive stages. This conditionality in the social life of P. obesinymphae reveals complex dynamics and a degree of behavioral plasticity not previously known in aphid societies.

Figure 1

Clonal variation in a P. obesinymphae gall, subdivided by developmental stage of resident aphids, revealed by PCR-restriction fragment length polymorphism (see Materials and Methods for details). All gels contained a 100-bp ladder as a size standard, followed by the gall foundress (F) and the larvae being tested against the foundress: those in the nondefensive, reproductive stages (lanes r1–r6) and those in the first-instar soldier stage (lanes s1–s14). Lanes C1 and C2 are control genotypes previously typed by direct sequencing. In the absence of intruders, all individuals would share the same genotype, which is identical to the clone foundress. Thus, nymphs of P. obesinymphae clearly move between galls, and intruders tend to accelerate development once they become residents in nonnatal galls.

Figure 2

(a) Percentages of intruders defending colonies (black bars) compared with the overall percentage of intruders in the same colonies (white bars). (b) Percentages of nonreproductive soldiers in colonies that were intruders (black bars) compared with the percentages of reproductives that were intruders in the same colonies (white bars), based on assays of the SNP marker. Note that categories are independent samples and, thus, should not sum to 100%, and that assays of behavior and development were not made on the same colonies. Both comparisons support the interpretation that intruders behave selfishly by parasitizing the altruistic tendencies expressed by unrelated, natal clones (a, P = 0.002; b, P = 0.015; paired t tests on arcsine–square root transformed proportions).