The Early Superorganism Concept
It has long been noticed that durable social groups have a certain structural similarity with individual animals. In this view, any society can be regarded as a “superorganism”, effectively an organism made up of organisms. This concept was first made explicit in sociology in the late nineteenth century – think of the long-standing expression body politic – and not long afterward was applied to social groups of nonhuman animals.
As applied to social insects, the analogy has given rise to such terms as colony, drone, queen, slavery, soldier, and worker. The analogy was treated as a more or less casual metaphor until, about a century ago, the world’s leading specialist on ants, William Morton Wheeler made a strong case for applying it to social insects . He noted that the colony resembles a metazoan body in a number of striking ways. Among these, it shows a division of labor among its constituent members and a colony cycle mirroring the individual life cycle of birth, growth, maturation, reproduction, and finally death. He further characterized the reproductive individuals as the colony’s germ-plasm and the workers as its soma, and analogized the different subcastes of workers with particular metazoan tissues and organs. Especially in popular writings, there developed a fashion to identify parts of the colony or nest as the society’s “skeleton” or “liver” or “respiratory system”.
However, to Wheeler, the superorganism concept was more than a metaphor for thinking about social insects. He stated not just that the colony resembles an individual organism but that it is an organism. As such, he envisioned an immensely promising practice of physiology on the level of the colony. Ant colonies, especially, are readily kept and manipulated in artificial observation nests, so that a particular caste or subcaste can be increased or reduced in number or transferred between colonies, something that is not readily done with the organs or tissues of an individual animal. He believed that the exploitation of the superorganism in this way would usher in a promising new era in whole-colony physiology (much later named sociophysiology) that might well go beyond aiding in the understanding of animal societies to throw light on single-organism physiology.
Despite this apparent bright outlook, the superorganism concept of the early twentieth century fulfilled virtually none of this promise. Wheeler, himself, was not an experimenter and did little after his key paper to promote its application. Those who were experimenters all but ignored what he saw as the concept’s potential, so that it remained in the realm of theory – and often as little more than an occasional pleasantry or even proven truism – until in the 1950s, it all but vanished from view as a real scientific project.
Enter the Late Superorganism Concept
Then, in the 1980s, the social-insect colony as a superorganism reemerged rather prominently onto the scientific agenda, where it has remained to this day. It is sometimes suggested that this represents a revival of the concept of the early twentieth century, but it is hard to take this seriously. Despite the synonymy and a gross similarity, it is better to treat Wheeler’s early superorganism concept and today’s late superorganism concept as quite different creatures. There is no evident indication that later authors drew any inspiration from the early concept or that they would have proceeded differently if it had not existed. A big book titled The Superorganism  makes hardly any reference to the early superorganism concept, much less any suggestion that late superorganism concept is rooted in it.
What, then, sets the two supeorganism concepts apart? The most salient difference is that the late concept does not take the analogy nearly as literally in its details. Those writing about the early concept often analogized organisms and superorganisms in a rather literal manner. Today there are occasional remarks along this line (e.g., Ref. : Table 5-1, a set of ten “functional parallels between an organism and a superorganism”), but they are not central to the analysis and seem not even to be taken very seriously. The question of which part of a colony serves as its stomach or white blood cells, for example, is almost absent from a concept whose basic premise is that the colony is a system of processes with some resemblance to those in a single organism. Furthermore, it is claimed that the late concept exists in at least three different forms, none with any particular unity with the early concept and that only the early concept has an organic connection with major evolutionary transitions that the late concept lacks .
As an example of the application of the late superorganism analogy, in humans and other vertebrates fever is the body’s way of combating heat-sensitive pathogens. Such pathogens also infect insect societies, some of which have a marked ability to control temperature inside the nest, which suggested colony-level fever as a possible response to infection by heat-sensitivity pathogens. From this, it is experimentally demonstrated that honey bee colonies induce fever in just these circumstances .
As a further example, it is found that in its collective mass, a large colony scales much like an animal with respect to metabolism and longevity . These results seem consistent with the expectation of colony-level adaptations.
A key difference between the colony and an animal of similar mass lies in the organization of its activities. Even centuries ago, it was occasionally remarked that the honey bee “queen” is in fact a mother with little involvement in directing the colony’s activities. The question of who, then, was in charge, long remained unanswered. Today there is a robust consensus that the often very impressive colony-level activities are decentralized and self-organized in a manner much more akin to the internet than any organization with a chain of command. This has given rise to the term “swarm intelligence” , which has been taken over as a model in artificial intelligence studies.
A Clash of Paradigms
The late superorganism concept has become more than a source of testable predictions. It can also serve as a paradigm of the colony [7, 14]. In one definition, “The superorganism is a colony of individuals self-organized by division of labor and united by a closed system of communication. Its members choose their labor roles by a small number of relatively simple algorithms that evolved by natural selection at the colony level.” 
In what amounts to a very accessible manifesto for this view, the thesis is set forth that eusociality in insects originates through a very uncommon “combination of progressive provisioning with environments of the kind that give an edge to group selection over individual direct selection, causing offspring to stay at the natal nest rather than disperse,” 
The alternative view of the colony before us at present – which we can call the kin-selection paradigm – treats it not so much as a kind of organism but as a group of individuals with varying patterns of relatedness. These unavoidably give rise to conflicts of interest within the colony, which along with their resolution form an important area of inquiry. This is not to suggest that proponents of the late superorganism concept are unaware that the colony is not a clone, as seems to have been overlooked in the early concept. However, they note that natural selection can operate at more than one organizational level, claiming that selection at the whole-colony level can be strong enough to over-ride that at the individual level. Likewise, it should not be supposed that proponents of the alternative view consider kinship patterns the sole driver of social evolution. It is recognized by all that in the absence of particular ecological conditions group living cannot evolve.
Are these two paradigms in conflict with each other? Very much so . Recent literature has seen a series of arguments that fall clearly divided into two parties. On one side – taking the more conservative position in the present context – it is argued that kin selection is the key to understanding not only the origin of sociality in insects but its continuing evolution and manifestations (e.g., Ref. ). The other, insurgent side maintains that kin selection is at most a side-issue and that colony-level group selection explains why colonies of social insects originated and are as they are. Note that the central importance of altruism at the level of the individual is not disputed. Rather, it is a question of how it can and does evolve.
It is likewise undisputed that social-insect colonies almost always consist of close kin. It might seem obvious that this fact speaks to the kin-selection paradigm, but it has been suggested that this is an outcome of eusociality, instead of a cause [17, 19]. However, this suggestion has been effectively put to rest, at least as far as the Hymenoptera are concerned, by a phylogenetic test showing that monandry (single mating by the queen, so that her daughters are full sisters) is in the ground plan of all independent eusocial lineages .
In an earlier time, proponents of the group selection paradigm might have allowed a key role for kin selection at the origin of eusociality , while arguing that it has little place in the “ultimate superorganism” and comparable colonies. However, at present, even this is not conceded in the view that, while altruism is a critical component to any durable sociality, kin-selected altruism is not at the heart of the evolution of sociality in insects [8, 18, 19]. As another expression of this view, “Multilevel selection theory shows that groups can evolve a high level of functional organization when between-group selection predominates over within-group selection.”  Kin selection theory, in this view, is not demonstrably mistaken, just ineffective in advancing our understanding of the origin and further evolution of insect sociality in nature. Furthermore, it is suggested that “Inclusive fitness theory has retarded understanding in a number of important respects.”  Among others, “it misleadingly suggested that genetic relatedness is the primary factor that explains the evolution of eusociality, distracting attention from [ecological] factors of greater importance.”
This controversy was brought to its critical point by a paper advancing the group-selection argument on the basis of mathematical models of conditions leading to sociality under kin selection versus those under group selection . In what amounts to an argument from parsimony, the conclusion was a claim to provide the mathematical underpinnings to the earlier view of group selection as a strong binding force in social evolution, versus kin selection as at most a weak binding force . Furthermore, Nowak et al.  concluded that very little of the impressive progress of recent decades in understanding social organization in insects was due to kin-selection theory. This paper unleashed a sharp debate in the pages of Nature (1, 3, 4, and others) that involved many of those working on the evolution of social insects, including 22 contributors to this volume. Among other things, the claim of kin-selection theory’s lack of productivity was countered by lists of behavioral phenomena illuminated by the theory and areas in which it had provided testable predictions (Ref. : Tables 1 and 2).
At present, the debate seems largely to have died down, not because there is any real resolution but because the two sides have agreed to disagree.
Given this situation, how do the proponents of two competing paradigms relate to each other within the scientific enterprise? Students of the history of science might expect either that one paradigm would defeat the other and drive it into retreat (as in the controversy around phenetic systematics versus cladistics a generation ago) or that they would separate into separate organizations, each with its own conferences and journals (as with psychiatry and psychoanalysis). Remarkably, nothing of the sort has taken place. Instead, the two competing paradigms are found side-by-side within the International Union for the Study of Social Insects, its conferences, and in Insectes Sociaux and other journals.
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