Comparative phenotyping across a social transition in aphids

• We compared ecological and behavioural traits of Pemphigus aphids across a social transition.
• Sociality in aphids did not occur as discrete polyphenic traits, but rather varied continuously.
• Sociality-associated behaviours (e.g. housekeeping, defence) varied across aphid species.
• We used an objective measure of aphid sociality: natural predator morbidity.

In some insects, eusociality has evolved independently more than once, such that closely related species differ in the presence or absence of altruistic traits. Such groups offer opportunities to study the ecological and evolutionary drivers of transitions to sociality. In Pemphigus aphids, for example, eusociality has evolved independently multiple times, but most species are assumed to be nonsocial. Eusocial aphids thus typically have close relatives that are nonsocial, indicating a rapid and distinct transition to sociality. However, there has been only limited study of the behaviour of nonsocial species that permit direct comparisons with eusocial species. In this study, we characterized three aphid species along two axes of social behaviour: housekeeping and defence. Previous evidence suggested that these three species differ in the presence or absence of social traits. We found that for the ecological and behavioural traits we tested, there were quantifiable differences between social and nonsocial species. However, there was no clear threshold that differentiated social from nonsocial species, meaning that definitions of sociality in aphids depend in part on the traits that are measured. If sociality is measured by defence, for example, the eusocial species, Pemphigus obesinymphae clearly expressed the greatest degree of aggressive and effective defence. However, some defensive behaviour was also present in the species traditionally defined as nonsocial. Conversely, if sociality in aphids is measured by traits related to homeostasis and housekeeping, then the species traditionally considered nonsocial expressed nearly the same behaviours as the eusocial species. These results imply that sociality in aphids evolves as a collection of uncorrelated traits. Clear analogues or antecedents of more derived social characters can be identified in species that are nominally nonsocial.