What is it about ants that allows us to speak of their societies as "superorganisms"? In my view, one issue is fundamental: colony members share a permanent and unshakable bond as a group.
Often the word “superorganism” has been used merely to indicate that ant colonies are complex in some way, or that they show features similar in some way to those of a single organism. Most such applications of the word are not especially enlightening. It is true, for example, that the labor pool of different castes in a colony might be compared to organs in a body, but anything of sufficient complexity is likely to be composed of subunits in this way, such as a car with its engine and wheels.
These conceptions of superorganism also ignore nature's diversity. Simple multicellular organisms-- and no one disputes they are organisms--have no organs, no division of labor, and no overlap in generations among their constituent parts (they are composed of equivalent cells that live and die together). And though there is a pleasing analogy between the differentiation of the ants in a colony into reproductive and worker castes and the differentiation of the cells in our bodies into reproductive and somatic types, the great majority of organisms do not have a set germ line of this kind. Therefore such characteristics of ant colonies as the existence of queens and other labor specialists, communal nourishment of the young, and the presence of multiple generations living together, while they parallel characteristics of a human body, are not essential traits of organisms. It is unclear then why we would require them to be essential criteria for superorganisms -- a term that after all was introduced to make a comparison to organisms in general, not just vertebrate or human bodies.
When W.M. Wheeler came up with the term superorganism, he was thinking that ant colonies were organisms, plan and simple—not a particular kind of organism. Is there an diagnostic attribute universal to organisms that we could look for in defining superorganisms, too? Yes: the component cells of all organisms share a tight identification to the whole, giving them a sense of self and non-self. Other than the gametes and embryos that form new individuals under conditions specific to a species (each new individual with a novel identity), no part of an organism has the option to set up shop alone or defect to another individual. That’s true whether the organism is as simple as the Volvox shown below, or as complex as a person.
This means organisms are not “permeable” (to use a word Edward O. Wilson applied to animal societies on page 17 of his book, Sociobiology). That is true, for example, of sponges. It's sometimes said that sponge cells survive independently after the animal is passed through a sieve. Not so: lone cells last an hour or two (no longer than a human cheek cell might if scratched off with a fingernail and deposited on a moist spot). Their one chance of survival and propagation is to crawl together to resurrect the same individual. If two sponges are sieved at the same time, their cells sort themselves out to form the original individuals, with no cross-over.
This rule of lack of permeability and absolute identity with the whole is so universal that it can be used to define when group of cells constitutes an organism. Consider a cellular slime mold consisting of amoeba that have come together to travel as a group known as a "slug" (see the image below); roving bacteria do the same thing when they form a “wolf pack” (AAA, page 32). In both cases the individuals that compose the group can depart on their own, or transfer to another group. They lack an immutable sense of group identity. They are best not thought of as "organisms," but are rather a kind of herd (or "wolf pack," if you prefer).
It's identity that unites cells into an organism, conflict or not, complexity or not, division of labor or not. The advantage of this point of view is that we define organisms (and similarly, superorganisms) on functional grounds rather than on some characteristic thought to be important to their evolution, such as relatedness, as Brown University professor David Queller pointed out to me. This makes sense because "we should decide what's special about organisms, and THEN asks what makes them that way."
Ants show an commitment to the whole (their colonies) that is as absolute and unbreakable as it is for cells in organisms. As the book describes (AAA, page 229):
Thinking about superorganisms in this way focuses us on new questions about societies in general. Are there conditions under which the binding force can be broken, allowing society members to start their own colony or to join other colonies? If so, do such conditions occur only in the laboratory (much like cultivating cheek cells in a Petri dish--few would call such a cell culture a "human.") Or do such breakdowns happen in nature? And if so, is the behavior part of a normal colony cycle or a kind of disease or parasitism (as occurs, in the form of social parasitism, in slavemaking colonies)?
Here is an example of an unusual instance of colony merger in the ants: when incipient colonies of the fire ant Solenopsis invicta are invaded by superior forces, workers abandon their queen and join the larger nest. Walter Tschinkel hypothesizes that this is a ruse to permit their queen to live another day, and either found a colony from scratch or infiltrate the one containing her workers. By the logic of his proposed scenario, the identity of the smaller colony may actually remain intact.
What, then of other, more traditional ways of classifying animal societies? For more than 40 years, societies (and particularly those of social insects) have been described as "advanced" or eusocial when they show 1) a reproductive division of labor; 2) cooperative care of the young; and 3) an overlap in generations. These attributes are particularly valuable in studying groups for which they vary, such as wasps, but it is arguable whether they are fundamental criteria for sociality. It's no wonder the set of eusocial traits have never been pursued as critical subjects in studies of the nature of organisms. As we've seen, they don't necessarily apply to organisms (and therefore logically to superorganisms either, if we keep to the original intent of the word).
Being eusocial and being a superorganism therefore seem to be separate issues. Below I briefly review the information on group identity in eusocial animals, which suggests that superorganisms are scarcer than eusocial species, with the preeminent examples being the ants, and naked mole rats coming a close second. (Incidentally, while both ants and naked mole rats are eusocial, I don't see any reason that eusociality should be required for a group to develop the identity of a superorganism. Some of the "primitively social" species reviewed by Jim Costa need particular study in this regard.)
Paul Sherman tells me the naked mole rats, remarkable eusocial vertebrates with ant-like societies composed of a queen and workers, are incapable of transferring to another colony. (Occasionally a worker can change her role by leaving to start a colony of her own, but if one takes Wheeler's dictum that [ant] superorganisms are organisms seriously, this is not a problem: the tissues of many organisms such as fungi can shift from somatic to reproductive functions).
David Roubik informs me that while lone workers of social bees are incapable of reproduction and soon die, in many species they transfer easily to other colonies in a behavior called drifting, which occurs often when a worker becomes lost. This can happen also between species, both among honeybees and stingless bees.
There is less information on social wasps, but in at least some cases individuals can create their own groups from scratch, as Robert Jeanne tells me Polistes fuscatus wasps do each spring. Bob has also seen Polybia occidentalis individuals inveigle their way into another colony that is in the process of moving to a new nest location.
Eusocial aphid lack colony level recognition, and easily leave one group for another. Bernie Crespi tells me that eusocial thrips likewise have no colony recognition, and Holly Caravan, a doctoral student of Tom Chapman, is investigating whether soldier thrips can transfer between colonies. Though the situation in eusocial shrimps has not been studied, Emmett Duffy reports that individual shrimps move around a “surprising amount.”
At least some termites merge their colonies commonly in nature, often resulting in individuals from both groups reproducing together in one nest. During my visit to Namibia last year, Scott Turner told me how workers of Macrotermes mound building termites mix freely in the lab, suggesting that colony identity cues are lacking or easily confused in this highly evolved species. No one knows whether the colonies remain separate in nature by other means, perhaps through the foraging columns generally avoiding each other. In which case one might call the colonies "superorganisms" by a less restrictive definition (superorganism sensu lato).
Other nuances to the superorganism idea could be distinguished, for example colony borders might break down after the death of the queen in species where she is the source of identity cues. But generally I prefer a hard-line approach to the definition, even though it leads to unexpected results. Given how cooperative and harmonious their workers are, for example, it might seem radical to exclude honey bees as superorganisms just because they can join the wrong colony by error. The very fact foreign individuals are accepted into a healthy bee colony tells us the identification to the whole is less developed for bees in colonies than it is for cells in organisms: after a kiss, the lip cells of a lover cannot form colonies in a person’s mouth—this kind of transfer simply does not occur between organisms.
Are there ants in which individuals drift from colony to colony? Certainly the question needs study. One Australian species may occasionally show such behavior, and it is claimed that Lasius austriacus has lost colony identification entirely. Nonetheless, successful transfers seem to be extraordinarily rare or absent in ants, which therefore form supercolonies by virtually any definition.
Postscript, 19 June 2010, Part I: Do Superorganisms need to be Collections of Organisms?
Superorganisms are often described as if they must be comprised of collections of multi-cellular organisms (such as ant workers), in contrast to organisms, which consist of cells. The idea of identity as a shared and defining feature of both organisms and superorganisms suggests a different point of view: that the essential difference between the two is the mobility of their components. Worker ants can wander off on their own to (for example) search for food; whereas cells do not move away from and then later rejoin our bodies.
It's conceivable bacteria in a wolf pack could share an identity such that each could wander away something like an ant worker, and then rejoin the same wolf pack (and no other). This would make such a group a kind of superorganism consisting of single cells--a kind of union as yet unknown in nature.
Postscript, 19 June 2010, Part II: Cooperation versus Conflict
Some people continue to express the idea that cooperation versus conflict are useful as defining criterion for superorganisms. I find this surprising because conflict occurs regularly within organisms, including inside our own bodies (see page 228 of AAA), and the presence such conflicts has never had any bearing on our perception of human (or other) bodies as organisms. It's true that conflict can reach higher levels in healthy (?) societies than in a healthy organism, but this leads us to another issue: as with most other traits that have been proposed as defining a superorganism, cooperation and conflict vary over a continuum.
I addressed choices in word definitions when I wrote a review of the terminology of canopy biology for the Association for Tropical Biology a few years ago for their journal, Biotropica:
If pushed sufficiently hard, any definition outside those for mathematical terms and other abstractions will break down. Show me a car, and I might show you a pile of junk that once functioned as a car (and maybe in a mechanic's mind it still is). Show her a star, and an astronomer points to a mass of convergent superheated dust. The hallmark of a good definition is not entirely that it tidily delimits a set of X's, but that it also necessarily causes problems (breaks down) when things get conceptually interesting about X, as when the biological species concept presents difficulties for organisms undergoing the kinds of change Mayr (1963) considers pivotal to the generation of new species, or when a parasitic plant starts to resemble a mutualist.
So the question is this: If we use cooperation / conflict criterion to define superorganisms, is it possible to select a particular cutoff point within the continuum of possibilities that is conceptually exciting, rather than arbitrary? That would be a robust definition. We should also ask, can such a definition be aligned with the intended comparison to organisms? If not, it should be applied to a different word than "superorganism."
This essay expands upon ideas in the Conclusion of AAA, especially page 229.
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