Army Ants Trapped by Their Evolutionary History

R eading the French version of Journey to the Ants by Bert Hölldobler and Edward O. Wilson (1996) during the course of my graduate studies, I remember being amazed by the description of circular mills formed by an isolated group of army ants. This phenomenon occurs when a group of foragers is separated from the main column of the raiding swarm by a perturbation of their pheromonal communication (Schneirla 1944). The separated workers then run in a densely packed circle until they all die from exhaustion (Schneirla 1971). As a student in evolutionary biology, I was puzzled by how such an apparently aberrant behavior could have originated and could be maintained during the course of evolution. This natural phenomenon is reproducible in the laboratory and has recently been shown to result from a self-organizing pattern (Couzin and Franks 2003). After a period of disorder, a random direction is collectively selected by ants, and a circular mill forms, following simple rules of motion governed by direct interactions between individuals. But now, a phylogenetic study by Seán G. Brady (2003) sheds new light on the origin of this behavior by showing that the answer to the apparent paradox of circular milling lies at least in part in the evolutionary history of these ants. In fact, the formation of circular mills is a somewhat extreme illustration of the obligate collective foraging behavior characteristic of army ants, which are ineffective at foraging solitarily. These species stage " swarm raids " composed of numerous workers foraging for prey, which is overwhelmed and brought back to the nest along dense traffic lanes. Army ant species are also nomadic—they construct temporary nests whose location depends on food resource availability. Queens of army ant colonies are highly modified relative to those of other ant species in being wingless and able to produce a huge number of eggs per brood cycle. These three characteristics—obligate collective foraging, nomadism, and highly modified queens—define what has been called " the army ant syndrome " of behavioral and reproductive traits shared by all army ant species. Until now, the dominant view was that this syndrome originated at least three times independently in army ant lineages, two restricted to the Old World (Aenictinae and Dorylinae) and one to the New World (Ecitoninae). This hypothesis implies that the army ant array of behavioral and reproductive traits has multiple origins and that their morphological and behavioral …