Abstract
BACKGROUND: Because the systems of social organisation in the various species of Pemphigus aphids span the continuum from asociality through to advanced sociality (typified by the possession of morphologically specialised soldiers), the genus is an ideal model clade in which to study the influence of ecology on the origins of eusociality. We made detailed study of the ecology of three gall-dwelling species that show clear differences in their levels of social behaviour. To elucidate evolutionary relationships and to attempt to estimate the number of origins of sociality, we also created a phylogeny based on sequences spanning the mitochondrial genes Cytochrome Oxidase I and II for nine species of Pemphigus. RESULTS: P. spyrothecae, a highly social species with aggressive morphologically-specialised soldiers, has the longest galling phase, unsynchronised development of a large number of individuals in a densely-populated gall, and an extended period over which alates emerge. P. populi, a species with no soldiers, has the shortest galling phase, synchronised development of a small number of individuals in a sparsely-populated gall, and an extremely brief emergence period. The ecology of P. bursarius, which has behavioural soldiers that are not morphologically specialised, is intermediate between these two extremes. The galls of P. spyrothecae and P. bursarius form small openings during the course of the season and predation-related mortality is relatively high in these two species. Conversely, predation does not occur during the galling phase of P. populi, which has no soldiers but makes an entirely-sealed gall. The phylogeny allowed us to infer one likely point of origin of basic social defence and two independent origins of enhanced defence. Based on current knowledge of behaviour, the phylogeny also suggests that the defence trait may have been lost at least once. CONCLUSION: The life-history strategy of P. spyrothecae appears to be geared towards defending the colony against the constant threat of predation that faces the inhabitants of a long-lived, open gall. The life-history strategy of P. populi, on the other hand, is to avoid predation in the closed gall fortress and flee for the secondary host at the earliest opportunity. The life-history strategy of P. bursarius appears to represent a compromise between these strategies.