Polydomy: the organisation and adaptive function of complex nest systems in ants

Some ants have an extraordinary social organization, called unicoloniality, whereby individuals mix freely among physically separated nests. This type of social organization is not only a key attribute responsible for the ecological domination of these ants, but also an evolutionary paradox and a potential problem for kin selection theory because relatedness between nest mates is effectively zero. The introduction of the Argentine ant in Europe was apparently accompanied by a dramatic loss of inter-nest aggression and the formation of two immense supercolonies (which effectively are two unicolonial populations). Introduced populations experienced only limited loss of genetic diversity at neutral markers, indicating that the breakdown of recognition ability is unlikely to be merely due to a genetic bottleneck. Rather, we suggest that a "genetic cleansing" of recognition cues occurred after introduction. Indeed workers of the same supercolony are never aggressive to each other despite the large geographical distance and considerable genetic differentiation between sampling sites. By contrast, aggression is invariably extremely high between the two supercolonies, indicating that they have become fixed for different recognition alleles. The main supercolony, which ranges over 6,000 km from Italy to the Spanish Atlantic coast, effectively forms the largest cooperative unit ever recorded.

Unicolonial ant populations are the most extensive cooperative units known in nature, forming networks of interconnected nests extending sometimes hundreds of kilometers. Within such a supercolony, worker altruistic behavior might be maladaptive, because it seems to aid random members of the population instead of relatives. However, recent genetic and behavioral data show that, viewed on a sufficiently large scale, unicolonial ants do have colony boundaries that define very large kin groups. It seems likely that they are family groups that continue to express their kin-selected behavior as they grow to extreme sizes. However, at extreme sizes, kin selection theory predicts that these behaviors are maladapted and evolutionarily unstable, a prediction that is supported by their twiggy phylogenetic distribution.