Unicolonial ants: where do they come from, what are they and where are they going?

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.

Introduction

Dreamers have always sought harmony and cooperation in nature. The painter Paul Gauguin, for example, thought he could find it in untrammeled Tahiti. But nature, forged on the anvil of natural selection, tends to be selfish. Gauguin's voyage, ironically, took him away from one of the few types of natural harmonious societies, ants, because they are ill equipped to reach oceanic islands. Ants, like other social insects, have evolved cooperative societies based on kinship [1] (Box 1). But had Gauguin been able to wait longer, he would have seen Tahiti overrun with hypercooperative invasive ants such as Anoplolepis gracilipes, Pheidole megacephala, Solenopsis geminata and Wasmannia auropunctata [2]. These cooperate not just within the normal confines of a single nest and a single nuclear family but across the population as though it were a single colony. They are therefore described as unicolonial (see Glossary).

Unicolonial ants often turn their extreme cooperation into extreme ecological dominance. On Christmas Island, A. gracilipes has restructured the entire forest ecosystem [3]. Historical invasions of Caribbean islands, thought to be by S. geminata and P. megacephala, destroyed crops and made them nearly uninhabitable for a time [4]. Another such ant, Paratrechina longicornis, invaded and overwhelmed Biosphere 2, dashing its creators’ plans for a sustainable completely enclosed ecosystem (Figure 1) [5].

Gauguin was no evolutionary biologist, but the title of his 1897 masterpiece, ‘Where do we come from? What are we? Where are we going?,’ could be asked about any product of evolution, and unicolonial ants are particularly apt subjects. First, understanding what unicolonial ants are is not possible without understanding their past. Where unicolonial ants came from is a major puzzle because it is not clear how cooperation can evolve on this huge scale. Second, whereas evolutionary biology can rarely predict where any species is going, it does predict that, despite their short-term ecological success, unicolonial ants are an evolutionary dead end.