- Open Access
Do unicolonial wood ants favor kin?
© BioMed Central Ltd 2009
- Published: 18 June 2009
Vast supercolonies of interconnected nests formed by unicolonial ant species are the largest cooperative groups of animals known. Research published recently in BMC Evolutionary Biology reveals that a supercolony can be more genetically structured than previously thought, comprising several extended families. Surprisingly, the families coexist peacefully, even though they seem to recognize each other as non-kin.
- Inclusive Fitness
- Behavioral Rule
- Brood Care
- Family Cluster
- Territorial Aggression
The supercolonies formed by so-called 'unicolonial' ant species are huge cooperative groups – networks of interconnected nests that exchange individuals and share territory peacefully over extensive areas . In extreme cases, a whole population can comprise a single supercolony; for example, the largest supercolony discovered, the Mediterranean Argentine ant supercolony, covers 6,000 kilometers of Southern European coastline, and individuals accept each other as colonymates all the way from Italy to the Spanish Atlantic coast . A feature of supercolonies compared with the more usual family-based colonies of social insects is the free movement of individuals between nests, and the fact that each nest contains several queens. Consequently, the relatedness between nestmates approaches zero in the Argentine ant and many other species, both invasive and non-invasive . In other words, individuals that share a nest are no more similar genetically than would be individuals chosen at random from the whole population.
In contrast to the Argentine ant, supercolonies of indigenous European ants, such as certain species of Formica wood ants, are found in stable habitats such as boreal or alpine forests and are non-invasive. But like their invasive counterparts, these supercolonies cover large areas, and workers from distant parts of the supercolony behave unaggressively, like nestmates, towards each other . Holzer et al.  made a detailed genetic and behavioral study of three F. paralugubris supercolonies in the Swiss Jura mountains, which revealed that the supercolonies are not as genetically heterogeneous as expected, but consist of cryptic genetically related clusters of nests . These clusters define groups of individuals that are genetically similar at a level comparable to cousins, with the proportion of genes shared approximating to 0.125. These extended families are not sharply delineated, but can exchange individuals and genes.
Holzer et al.  suggest that such family substructures might enable workers to direct help to their relatives, and that this might help to maintain the trait of unicoloniality, in line with kin selection theory. However, the presence of genetically differentiated subunits raises the question of why there is no aggression within the supercolony, and why the clusters keep exchanging individuals. In theory, workers should exclude non-kin from sharing resources and receiving altruistic help. In other supercolony-forming species studied, within the supercolony aggression seems to be minimized by workers being unable to recognize whether an ant is close kin or not, but F. paralugubris workers behave unaggressively in artificial bioassay encounters even though they do seem able to recognize non-nestmates . In contrast to most supercolonial ants, aggression is rare in F. paralugubris, even towards individuals from other super-colonies. The workers seem to treat most conspecifics amicably, even if recognized as 'outsiders'. Does this mean that the potential inclusive fitness payoffs from the family structuring are not in fact realized? Is it possible that the peaceful strategy is itself favored by selection?
Indiscriminate acceptance is beneficial if the probability of encountering unrelated individuals is low. This is likely in F. paralugubris, because the population structure found by Holzer et al.  suggests that movement between the extended family clusters is limited. Of particular importance in this regard, Keller and colleagues previously found that the dispersal of queens in F. paralugubris is limited. This would help to guarantee that brood care by the young workers is directed towards relatives, even if the workers later disperse. Workers in F. paralugubris increase their inclusive fitness not by territorial aggression, but by rearing related queens and males that disperse and compete with queens and males from less related nests in other clusters over recruitment as a breeder . Holzer et al.  found that especially males are prone to disperse and spread genes across the clusters. In other words, relatedness will be above zero in the brood-rearing context, which is most important for inclusive fitness, even where territorial aggression is lacking (Figure 1). The current study by Holzer et al.  confirms previous findings by Keller and colleagues that family structures are more obvious in queens and the brood than in old workers in another supercolonial Formica ant . This suggests that young workers take care of related broods, even if they drift away from their relatives later in their lives. Whether similar patterns of genetic structure and behavior also occur in invasive supercolonies remains to be seen.
It is also worth noting that acceptance of non-kin in the context of artificial aggression bioassays does not necessarily mean that they are always accepted in natural contexts more directly connected to inclusive fitness. Favoring individuals that are likely to be relatives is adaptive only in contexts where the inclusive fitness benefits of discrimination are large. If competition for breeding places occurs mainly by the recruitment of sexuals into the breeding population, workers should be most prone to discriminate in contexts more directly linked to their inclusive fitness, such as behavior towards queens and males, and brood care [7, 8].
Thus, worker ants in Formica supercolonies might be able to direct the benefits of brood care mainly to the 'right' individuals as dictated by kin selection theory. The other side of the non-aggression coin is whether it is harmful to the rearing of related reproductives to allow strangers into the territory. As long as this does not harm the production of reproductives in your own nest, the risk of aggression is perhaps not worth taking. This might be the case when resources are abundant and the benefits of territorial defense are subsequently small. Wood ants tend aphids, a resource that thrives when ants are abundant, so resource limitation may not be too severe in their case . It will be very interesting to see whether the putative family clusters in wood ants also correspond to foraging areas and the flow of resources, and whether ants are more prone to discrimination at food sources, especially when resources are scarce. Study of nutrient flow within a supercolony of the Argentine ant has also shown that a seemingly uniform supercolony might actually consist of separate nest networks across which food resources are not shared . Ideally, relatedness should be measured at the level of such functional units, in both native and invasive supercolonies.
The problem of indiscriminate altruism demonstrates how complicated assessing the adaptive benefits of a behavioral strategy can be. In particular, we need to consider all the contexts in which a behavioral rule is applied. The ability to readily recognize and respond to environmental information is an important constraint on adaptation , and organisms are not always able to adjust their behavior to make an optimal response to a given situation. Instead, they might need to rely on rules that work on average. In the case of ant workers in a supercolony, the payoffs of behavioral rules need to be assessed across all the contexts in which they are used, over seasons, over the lifetime of the workers, but also over the lifetime of the supercolony.
There may be cases where workers in a supercolony seem to be in a dilemma. They are obeying the behavioral rules that made their family big and strong, but this has brought them to a situation where the rules no longer pay off. But this is only a dilemma for evolutionary theory if we assume that adaptation must always be perfect. The dilemma disappears if we consider the rules underlying the behavior. Even if the rules seem maladaptive in some cases, the evolutionary benefits may have already been reaped in another.
I thank Joan Strassmann, Dave Queller, Jes S Pedersen and Tobias Uller for inspiring discussions on unicoloniality, and Tobias Uller for comments on the manuscript as well.
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