PERSPECTIVE Eusociality: Origin and consequences Edward O. Wilson*† and Bert Ho¨ lldobler‡§ *Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138-2902; ‡School of Life Sciences-LSC 274, Arizona State University, Tempe, AZ 85287-4501; and §Theodor-Boveri-Institut fu¨ r Biowissenschaften (Biozentrum), Universita¨t Wu¨ rzburg, Lehrstuhl fu¨ r Zoologie II, Am Hubland, D97074 Wu¨ rzburg, Germany Contributed by Edward O. Wilson, July 12, 2005 In this new assessment of the empirical evidence, an alternative to the standard model is proposed: group selection is the strong binding force in eusocial evolution; individual selection, the strong dissolutive force; and kin selection (narrowly defined), either a weak binding or weak dissolutive force, according to circumstance. Close kinship may be more a consequence of eusociality than a factor promoting its origin. A point of no return to the solitary state exists, as a rule when workers become anatomically differenti- ated. Eusociality has been rare in evolution, evidently due to the scarcity of environmental pressures adequate to tip the balance among countervailing forces in favor of group selection. Eusociality in ants and termites in the irreversible stage is the key to their ecological dominance and has (at least in ants) shaped some features of internal phylogeny. Their colonies are consistently superior to solitary and preeusocial competitors, due to the altruistic behavior among nestmates and their ability to organize coordinated ac- tion by pheromonal communication. n eusociality, an evolutionarily ad- of groups will spread if the positive in- theory are difficult to relate to the com- vanced level of colonial existence, tergroup component of the altruists’ fit- plexities of tangible social phenomena. adult colonial members belong to nesses exceeds the negative within-group We suggest that each force can be two or more overlapping genera- component of the altruists’ fitnesses heuristically classified as binding or dis- I solutive in its effect on colony cohesion tions, care cooperatively for the young, (4–6). Altruism is defined as behavior and are divided into reproductive and that benefits others at the cost of the and either strong or weak in its relative nonreproductive (or at least less-repro- lifetime production of offspring by the power. The degree of relatedness, the ductive) castes. The phenomenon is well altruist. The forces that determine this similarity across the whole genome of marked and nearly confined to insects, outcome are group selection, the differ- individuals as a result of recent common especially ants, bees, wasps, and ter- ential survival and reproduction of en- ancestry, is a factor that biases the di- mites, where it has been subject to a tire cooperative groups as a result of the rection and strength of the forces. When large body of mostly specialized research frequency of the eusociality alleles in elevated, say by lower individual dis- scattered across disciplines from genet- each; individual direct selection, accru- persal rates, relatedness can bring alleles ics to paleontology. It has long been the ing from the differential personal sur- for presociality and eusociality together conviction of researchers on social in- vival and reproduction of each of the more quickly. If it brings such genes to- sects that common principles exist at the colony members; and kin (indirect) se- gether more frequently due to shared organismic and superorganismic levels, lection, which we define here in the microhabitat preference, mate choice, or thus between individual insects and the original narrow sense as the favoring or other biological traits, it can have the tightly integrated colonies they compose disfavoring by individuals of collateral same effect. Relatedness can also in- (1, 2). Parallels have been persuasively relatives, i.e., relatives other than per- crease variance in presocial and eusocial drawn between the self-construction of sonal offspring. The inclusive fitness of alleles among groups, thus quickening organisms from molecules and tissues the prescribing genotype, of individual the pace of colony selection. But relat- and that of superorganisms from inter- colony members and hence statistically edness is relevant only insofar as it acting entire organisms (3). The princi- the colonies they compose, is the nonad- affects the frequency of alleles that pre- ples can be further parsed into two ditive product of the three forces. The scribe social behavior. Eusociality arises segments of the time scale: the develop- definition of kin selection in the com- by the superiority of organized groups mental decision rules that assemble or- monly used broad sense, which folds in over solitaires and cooperative preeuso- ganisms and colonies in each generation individual direct selection as well, pro- cial groups. It can, in theory at least, be and the origin of these rules through duces results that are consistent with initiated by group selection in either evolutionary time. those from the narrow sense but intu- the presence or absence of close related- Focusing here on the second princi- itively less clear and less practicable in ness and, when close relatedness exists, ple, evolutionary process, we suggest application. It also leads to such con- also in the presence or absence of kin how three seemingly disparate evolu- founding statements as ‘‘solitary species selection. Conversely, eusociality cannot tionary phenomena can be causally evolve by kin selection.’’ When the arise without the driving force of group linked: the selection forces that generate broad definition of kin selection is used selection, regardless of the degree of and shape eusociality, the rareness of (offspring included), colony selection relatedness within local populations or the origin of eusociality, and the ecolog- and kin selection are reduced to just cooperative aggregations. ical hegemony of eusocial insects. alternative ways of viewing change in Group selection which with the addi- the frequency of eusociality alleles in tion of cooperative behavior becomes The Forces of Natural Selection a population structured by relatedness colony selection, is the result of the Research during the past half century (4, 5). This formulation raises basic interaction of entire groups with their has incrementally clarified the nature of theory to a high level of mathematical environments (6, 7–11), conditioned by the collective forces that create and inclusiveness and abstraction, but it de- the efficiency of their internal opera- shape eusociality. At the most basic parts from the earlier and very heuristic level, an allele or ensemble of alleles narrow definition of kin selection; fur- †To whom correspondence should be addressed. E-mail: prescribing phenotypic plasticity that ther, the dynamical terms of the pop- [email protected]. includes self sacrifice of some members ulation genetic models composing the © 2005 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0505858102 PNAS ͉ September 20, 2005 ͉ vol. 102 ͉ no. 38 ͉ 13367–13371 tions (12). It promotes harmony among group members and genetic fitness of the group as a whole, once colony level is attained, and its effect is thereby in- herently binding. Individual direct selec- tion and kin selection play out in the social interactions of the colony mem- bers. By pitting individual members and nepotisms against one another, individ- ual direct selection tends to reduce col- ony harmony and genetic fitness. De- pending on circumstance, kin selection can be either binding or dissolutive, the latter by competition among nepotistic subgroups. In all of this multilevel the- ater of evolution, the gene remains the unit of selection, whereas the target of selection can be the individual, the group, or nepotistic alliances or other- wise biased actions within the group. The Point of No Return An abundance of evidence suggests that the strength of the biasing role of relat- edness within a species depends on the stage of its social evolution. The key transition occurs at a point in colony evolution that can be conveniently Fig. 1. The two competing hypotheses of the origin of eusociality in insects and thence before the point called the point of no return (13). of no return. The first (A) holds that in the earliest stage, kin selection is binding, making close relatedness a key feature; if combined with group selection, kin selection favors primitively eusocial colonies in a Beyond this level, it is impossible, or population of solitary or preeusocial insects (far left). The second hypothesis (B), newly presented here, at least difficult and uncommon, for a holds in contrast that group selection is paramount as the binding force, and kin selection is minor or species to regress from the eusocial to absent as a binding force for the group as a whole and weakly dissolutive if it forms competing groups. a more primitively eusocial, presocial, Relatedness, in hypothesis B, is increased as group selection cleanses the dissolutive nepotisms effect of kin or solitary condition. selection. The empirical evidence appears to favor, but does not conclusively prove, B. When in evolution does eusociality become irreversible? We infer that this comes very early in the evolution of that The Origin of Eusociality stage and circumstance, but it does not condition, in particular when an ana- A key question remaining is whether, in join group selection from environmental tomically distinct