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Primer essentially a new kind of nest, and the oldest ones foraging organism built up of organisms of outside the nest. Just as cells are the old kind. more fixed in function, so are they Consider the famous honeybee more fixed in space. Social insects, Eusociality waggle dance. This dance, in contrast, are not physically performed by returning foragers, connected, and their colonies give David C. Queller1 and Joan E. tells other workers the direction us examples of organismal entities Strassmann and distance of rich food sources. that are dispersed in space. A final The colony benefits by exploiting important difference is the lack of Most biologists devote their the hard-won knowledge of those centralized control in social insect research careers to working out the foragers that find food bonanzas. colonies. Despite the controlling intricacies of how their favorite The dance is celebrated as a rare image conveyed by use of the term organism functions, how it example of symbolic “queen”, there is nothing like a processes energy, transmits communication between individual colonial brain. No individual information from one place to organisms, but it can also be perceives the state of the entire another, regulates metabolites, viewed as a part of a signaling colony and sends out instructions. gets rid of waste, builds itself, cascade of the larger Instead, actions are usually self defends itself and reproduces superorganism that regulates work organized by simple rules. Different itself. If one wants to step back according to the supply and individuals each have small pieces and consider what it means to be demand. If the supply of food is of information, which are an organism, it is obviously great, there will be more waggle integrated by the colony as a necessary to broaden one’s scope dancers stimulating more foraging whole. A returning forager doesn’t and to consider the full range of to harvest it. But that is not the know how many foragers and organisms. But an even broader only adjustment necessary. processors are at work. Instead, strategy is to consider entities that Foragers, with their knowledge of she just experiences an indirect have organismal properties but are valuable food sources, do not effect of those numbers — the time outside the realm of standard waste time processing the food, required to offload her nectar or organisms. Man-made artifacts but hand it off to another set of pollen — and acts accordingly. have long been mined for fruitful bees inside the hive. If a forager Despite these differences, the analogies about particular has trouble finding a processor key defining similarity remains; organisms and functions. bee, she begins a different dance, colonies are like organisms, but Computer viruses and artificial life the tremble dance, which both unlike anything in the non- programs also capture some activates bees to become biological world, with respect to important similarities. But perhaps processors and inhibits waggle their degree of integration and the best we can do in this area is to dancing. The result is a negative cooperation for the good of the study eusocial colonies. feedback system that allocates whole. The key question then is an Eusociality is a term coined to workers to foraging and processing evolutionary one. How did this cover ants, bees, wasps, and tasks according to need (Figure 1). organismal degree of cooperation termites that have three Additional links in the system evolve, given that the Darwinian properties: overlap of include the needs of the brood and norm is closer to a struggle of all generations, cooperative rearing the degree to which storage against all? This is a question that of young and non-reproducing capacity is filled. Such regulatory doesn’t trouble us much for most worker castes. Other organisms feedback systems operate in multicellular organisms. Genes in a that have these traits have since nearly every aspect of social insect macrophage can easily be selected been added: some aphids and colony functioning, just as they do to cause their cells to specialize on thrips, a beetle, some snapping in other organisms. non-reproductive tasks, because shrimp and the naked mole rat. In Besides the clear similarities they are the same genes that will eusocial species, non- between organisms and be transmitted through the germ reproductive workers care for the superorganismal colonies, there line. This is ensured by clonal young of the reproductive queens are some differences that show us descent from a single-celled (and sometimes kings). As such, that entities with organism-like zygote. William D. Hamilton workers are analogous to the functionality and integration can showed that the same kind of somatic cells of an organism, operate in unfamiliar ways. For explanation applies to eusocial which work for the transmission example, the cells of organisms insects, but in a less absolute way. of their genes by proxy, via the terminally differentiate into Members of social insect colonies germ line cells. Like the cells of numerous specialized types, while are relatives, sometimes just a an organism, the members of a social insect colonies have at most single queen and her progeny. eusocial colony have evolved only a few terminally differentiated Therefore, though they are not elaborate mechanisms to castes. Instead, much of the clonal, the do share a large fraction enhance the survival and division of labor is carried out by of their genes. A gene causing self reproduction of the larger unit. means of a temporal specialization, sacrifice can thus be favored by The colony consisting of one or often with the youngest adults selection if it aids relatives who more queens and workers has tending the brood, older ones might bear copies of the gene, but been called a superorganism, carrying out other activities in the the aid has to be large enough to Current Biology Vol 13 No 22 R862

expansion in this area, it may be Nectar Nectar better to stay at home and help Search collecting processing than to take the risks of dispersing time rate rate to find a new home. Fortress defenders would include aphids and thrips that live in plant galls, termites that inhabit wood, the social shrimp that live in sponges, Number Number and the naked mole rats in their Waggle Tremble of of food dancing dancing extensive subterranean tunnel foragers storers systems. In contrast, life insurers, which may include most ants, bees, and wasps, forage outside Current Biology their nest to bring food back to their helpless young. This is a Figure 1. difficult lifestyle to follow as a Regulatory network controlling allocation of honeybee workers to nectar gathering solitary individual, because outside the hive and nectar processing within the hive. After Figure 6.14 of Seeley (1995). foraging entails risks of predation, and the death of the adult means compensate for the chance that had evolved over a dozen times in the death of all her dependent the aided relative does not carry a the Hymenoptera as against once young. It works much better when copy of the gene. So honeybee or twice in the diploid termites, and groups of adults share the risk; if workers can gain by stinging large also why workers are only female one dies, her investments in young vertebrate intruders, because they in the Hymenoptera, but both are not wasted because the may save their whole colony full of sexes in the termites. surviving adults can carry on. relatives who pass on the genes This elegant hypothesis Despite the organismal quality of for stinging. They have even dominated discussions of the eusocial colonies, there are limits evolved barbs on their stingers that evolution of eusociality for many to cooperation. If the worker increase the effectiveness of years, but has been weakened by honeybee’s use of her sting wins stinging by anchoring tightly in the further analysis. Once models prizes for altruism, the young victim, even though it also incorporated all the details of honeybee queen puts her sting to disembowels and kills the worker. reproductive value, sex ratios, and a strikingly different use. Honeybee This selection via effects on especially the fact that a female’s colonies reproduce by splitting. relatives, known as kin selection, is high relatedness to sisters is The old queen departs with the quantified in Hamilton’s rule, the countered by an unusually low majority of the worker force (Figure simplest version of which is c < b*r. relatedness to brothers, it became 2), leaving the remaining workers The fitness cost for the altruist (c) evident that any haplodiploid to await the emergence of several must be less than the fitness relatedness effect was not only new queens, who have been benefit to its relative (b), multiplied smaller than had been thought, but developing in specially prepared by the relatedness (r). In diploid transitory. Even though Hamilton’s cells. If the worker force is still species, the relatedness is 1/2 to specific haplodiploid hypothesis quite large, the first new queen to mothers, fathers, children, and full has been weakened, his general emerge may also leave with some siblings; it is 1/4 to half siblings, theory of kin selection remains of them to start another colony. If, uncles, aunts, nephews and central to the understanding of the however, the worker force is nieces, and so on. Hamilton also origin of eusociality. However, the smaller, the new queen stays and noticed that these relatedness focus has shifted from kin selection battles to the death with her sister values do not all apply to the ants, driven by unusually high queens for the right to set up bees, and wasps. These taxa are relatedness to kin selection with housekeeping in the old colony. members of the order normal relatedness, but driven by This too makes sense within the Hymenoptera, which has a unusually high benefits to relatives. calculus of kin selection. If there haplodiploid genetic system. Males Specifically, if relatedness to one’s are only enough workers to develop from unfertilized eggs and mother’s offspring is no higher than support one queen, then any are therefore haploid. Males relatedness to one’s own offspring, queen that gets rid of her rivals will bequeath their genes only to then a potential worker should help pass on more genes. The queens daughters, but they bequeath all of only if, for some reason, she can are related, which can limit them, the usual halving due to do more for her mother’s offspring selfishness, but only up to a point. meiosis being absent. As a result, than for her own. If a queen’s choice comes down to the daughters are related among Perhaps the two most important her own reproduction versus an themselves by 3/4. So, Hamilton classes of benefits to helping are equal amount of reproduction by reasoned, a female could pass on those called fortress defense and her sister, who is related by 1/4, more of her genes by trading her life insurance. Fortress defenders she will obviously pass on more own offspring, related by 1/2, for are eusocial species that live and genes if she can kill her sister. the more related sisters. This feed inside a protected area. As How eusocial insects deal with seemed to explain why eusociality long as there is space for conflict has been a major focus of Magazine R863 research in recent years. The while, when the old queen dies or fighting honey bee queens provide when the colony divides in two. The clues to both the cause of conflict sensible strategy for the colony is and its control. The greatest the one followed by honeybees: potential source of conflict is the produce just a queen or two at question of who gets to reproduce. those times. But in a Melipona Even though kin selected benefits colony, about 20% of all females can select for individuals helping develop into queens. Nearly all of rather than reproducing alone, it is them fail to reproduce, but for each better still to be the one being it is worth the risk for the small helped. The control of honeybee chance at the very high fighting is less visible, as you see it reproductive payoff of heading a not in the fights observed, but colony. For other colony members, rather in the peace that usually however, each excess queen is just Figure 2. prevails. The fights are deadly but a useless tax on colony resources, A swarm of honeybees en route to rare, because the number of new and so the workers kill them in founding a new colony. The old queen goes with the swarm, leaving young queens is limited to a few order to minimize the losses. queens to fight over the old colony. individuals at the time when they Thus, physical control is Photo courtesy of Thomas D. Seeley. are needed. Queens are raised in employed in both cases that lack special, large cells, and receive nutritional control. However, there shows both kin selected special food. Thus, the vast is an important difference: In the cooperation — formation of a majority of females are forced to small Polistes colonies, usually sterile stalk to help the spores become workers and are comprising no more than a few disperse — and cheating among morphologically unprepared to dozen individuals, the queen keeps different clones. Second, standard contest for the queen role. her subordinates in line. This would organisms have other conflicts, not Nutritional control is at the root of be difficult in the larger colonies of between their cells, but between queen-worker differentiation in Melipona, which can have many genes. For example, meiotic drive most social insects. thousands of individuals; in this genes gain excess representation What if this control was lacking? case it is the workers as a group in gametes while imposing a cost There are two natural that take charge of killing the on the organism as a whole. ‘experiments’ that reveal the excess queens. Likewise it is Organellar genes that pass through answer. The first comes from so- generally the workers who control eggs but not sperm can bias sex called primitively eusocial insects, food in species in which nutrition ratios toward daughters, or like Polistes paper wasps. These determines caste. This echoes the sabotage male function in have never evolved conclusion that we reached earlier hermaphrodites. Transposons and morphologically distinct queen- about the regulation of task other kinds of junk DNA can worker castes and in this respect performance being accomplished spread even if they are presumably resemble a eusocial only by the actions of numerous disadvantageous to the organism. line early in its evolution. In a individuals, rather than by Thus, eusocial insects have helped Polistes colony, there is still a centralized control. Reproduction teach us that organismal dominant egg layer or queen, but may be centralized in the queen, cooperation is not a given, that it her position is held by force or but in large colonies the control of required the evolution of ways to threat of force. Subordinate wasps who reproduces is exerted largely control reproductive conflict, and challenge her, and if the queen by the worker collective. that such control remains weakens, the next wasp in the One might argue that these imperfect in all organisms. hierarchy supplants her. conflicts give lie to the assertion The second natural experiment that eusocial colonies are Further reading Bourke, A.F.G., and Franks, N.R. (1995). comes from the stingless bee organismal. After all, one neither Social Evolution in Ants (Princeton genus Melipona, which belongs to expects nor observes such University Press). the same family as honeybees. conflicts among the cells of a Hölldobler, B., and Wilson, E.O. (1990). Here, queens and workers develop multicellular organism, because The Ants (Cambridge: Harvard University Press). in sealed cells, on essentially equal they are all clonal descendants of Queller, D.C., and Strassmann, J.E. provisions. They are, therefore, the zygote. But the study of (1998). Kin selection and social about the same size, but they have cooperation and conflict in social insects. Bioscience 48, 165–175. different proportions, with workers insects has taught us that we can Seeley, T.D. (1995). The Wisdom of the Hive (Cambridge: Harvard University being larger at the work end of the sometimes expect conflict in Press). body – the head and thorax – and organisms. For example, there are Szathmáry, E., and Maynard Smith, J. queens larger at the reproduction organisms whose cells are not (1995). The major evolutionary end, the abdomen. Because always clonal. In cellular slime transitions. Nature 374, 227–232. feeding does not control caste molds such as Dictyostelium 1 choice, each developing female discoideum, multicellular fruiting Department of Ecology and Evolutionary Biology MS-170, Rice gets to decide on her own fate. As bodies are formed by aggregation University, P.O. Box 1892, Houston in honeybees, a new Melipona of starving cells, sometimes from Texas 77005-1892, USA. E-mail: queen is needed only once in a different clones. This species [email protected]