Abstract: One of the most vigorous controversies in twentieth-century evolutionary biology concerns the question of whether selection operates on groups of organisms. Although explanations of biological phenomena in terms of "the good of the group" were common in the scientific literature prior to the 1960s, by the end of the decade such explanations had been abolished from evolutionary biology. Nonetheless, group selectionism has made a remarkable comeback in the last two decades. This article reviews some of the history of this debate, and then considers the contemporary status of group selectionism.
 

Introduction

In the "Introduction" to the Origin of Species Darwin provided perhaps the best concise statement of the theory of evolution by natural selection anyone has ever given:

Throughout much of this century, however, biologists routinely appealed to explanations of biological phenomena in terms of the "good of the group" or the "preservation of the species" -- explanations that seemed to presuppose that selection also operates at the level of these more inclusive entities. The idea that selection operates on groups of organisms -- group selectionism -- finally received serious critical scrutiny in the 1960s. It did not fare well. Prior to this decade group selectionist explanations of biological phenomena were common in the scientific literature. By the end of this decade such explanations had become rare. For all appearances group selectionism seemed dead. Yet in recent years group selectionism has enjoyed a surprising resurgence, and has inspired a new round of controversy. This article will review some of the history of this debate, consider the issues dividing contemporary disputants, and speculate a bit about the future of group selectionism. As we will see, group selectionism's uncertain future is in large measure a consequence of its troubled past.

The Watershed for Group Selectionism

A basic fact about nature, the importance of which had been recognized since Darwin, is that although even relatively "slow" breeding animals are physiologically capable of increasing their numbers at a stupendous rate, under normal circumstances their populations remain remarkably stable. Why? According to V.C. Wynne-Edwards, in his book Animal Dispersion in Relation to Social Behaviour [3], population numbers remain stable because animals actively regulate their population densities by modulating their reproductive outputs in relation to available resources. Wynne-Edwards realized that natural selection operating solely at the level of individual organisms would favor organisms that maximize individual reproductive success without regard for group welfare. He noted that such unrestricted reproduction would eventually lead to overexploitation of the habitat, population crash, and extinction. Because such occurrences are rare, he reasoned that another evolutionary force must be operative, one that is responsive to effects at the level of the whole group. Wynne-Edwards hypothesized that groups with social conventions for regulating population density will tend to go extinct less often than groups in which individual reproductive rates are insensitive to overall population density. Population-regulating groups will thus tend to persist longer, and may colonize areas left vacant by groups not exhibiting such reproductive restraint. Wynne-Edwards thought such "group selection" (as he called it) to be pervasive in nature, and indeed to lie at the base of all social behaviour.

Wynne-Edwards' emphasis on the subordination of individual advantage to group benefit reflected a long-standing and widely accepted explanatory tradition in ecology. Ecologists routinely assumed that selection operates to insure the well-being of biological entities more inclusive than individual organisms, and tended to talk about the adaptations associated with populations, species, and even multi-species ecological communities. [4] Unfortunately, this liberal approach to understanding the operation of natural selection conflicted sharply with the way that biologists influenced by the "modern synthesis" of evolutionary biology in the 1930s and 1940s approached evolution. For such biologists, selection acts at the level of individual organisms, no higher, and is best represented by models depicting changes in gene frequencies within populations. [5] Not surprisingly, the strongest criticisms of Wynne-Edwards' theory came from biologists influenced by this tradition, most notably by John Maynard Smith, David Lack, and George C. Williams.

A basic problem with Wynne-Edwards' theory, Maynard Smith argued [6], is that it postulates groups consisting entirely of individuals who abide by social conventions and altruistically limit their own reproduction for the sake of achieving population homeostasis. But whenever a group of altruists is "infected" by an individual (or gene) pursuing the anti-social (selfish) strategy of seeking to maximize individual reproduction, such an individual will have an advantage over its altruistic rivals and hence its strategy (by being passed on to its more numerous offspring) will quickly spread through the group. Groups consisting of altruists are thus always vulnerable to subversion from an anti-social invader (a "free-rider") who benefits from the social arrangement but contributes nothing toward its maintenance. Social arrangements of the kind required by Wynne-Edwards' theory are inherently unstable, and are thus unlikely to be realized very frequently in nature. Although Maynard Smith found fault with the theoretical basis of Wynne-Edwards' view, he did not, however, offer an alternative (non-group selectionist) explanation of "population regulation," the problem with which Wynne-Edwards had begun.

This task fell to David Lack. [7] In criticizing Wynne-Edwards' view that animals limit their reproductive output in order to preserve food resources, Lack drew heavily upon his own research into the factors governing clutch-size in birds. Individuals of each species lay a characteristic number of eggs in each breeding cycle (for example, the species-specific clutch-size for swifts is three). Because the reproductive rate would seem to be directly related to the number of eggs in each clutch, it may be asked why the individuals of particular species do not lay more eggs than they typically do. Wouldn't laying more eggs result in more offspring? Lack argued that breeding pairs of at least some species produce as many viable young as possible. But the key word here is viable. His experiments showed that even under very favorable conditions, swifts that laid clutches of three eggs fledged more offspring than those who laid four eggs. Further experiments showed that the upper limit of clutch-size is set by the fact that when more young than this are produced, parents are unable to find enough food for all, so that increased mortality reduces the total number of offspring reaching maturity. Lack concluded that there is a sense in which animals limit their own numbers, but they do so, not for the good of their group, as Wynne-Edwards supposed, but rather to enhance their own individual fitness. "Population regulation," Lack argued, is simply an effect of organisms striving to maximize their individual fitness in resource-limited environments.

Finally, George C. Williams delivered what many biologists consider to have been the fatal coup de grace to Wynne-Edwards' theory. [8] The primary motivation for considering selection at the level of the group is to explain apparently adaptive features of biological systems that resist explanation in terms of selection operating among individual organisms. Williams argued that the sort of group adaptations Wynne-Edwards thought needed to be explained in terms of group selection could be explained more parsimoniously as the statistical effects of selection operating on individual organisms. Schooling in fish, for example, should be explained, not as a means for fish to assess the density of their population and to adjust their reproduction accordingly, as Wynne-Edwards supposed, but rather simply as the cumulative effect of the selfish behaviour of individual organisms, each of which uses the bodies of its schoolmates to create a buffer between itself and any predators lurking nearby. Other supposed group adaptations could be disposed of in similar ways. But if so, then group selection, which was introduced to explain group adaptations, could be dismissed without further adieu. Although not the last critique of Animal Dispersion to appear in the 1960s, Williams' arguments convinced many biologists that group selection of the sort that Wynne-Edwards considered pervasive in nature was a chimera. As D.S. Wilson has noted, by the end of the decade "group selection rivaled Lamarckianism as the most thoroughly repudiated idea in evolutionary theory". [9]

The Revival of Group Selection

Despite its apparent demise, group selectionism did not stay dead for long. In the 1970s group selectionist thinking "mysteriously rose from the dead". [9] Revitalizing ideas first developed by Sewall Wright in the 1930s, Wilson and others developed new models of group selection that attempted to avoid the difficulties facing Wynne-Edwards' model by incorporating more biologically plausible assumptions about population structure. According to standard population genetics models, individuals within a population (or "deme") are assumed to interact at random, with every individual having an equal chance of encountering every other individual. As Wilson pointed out, however, on a daily basis individuals usually encounter only a small proportion of the population to which they belong. Rather than being spatially homogeneous with respect to interactions, most demes display a good deal of internal structure. Wilson's "structured deme" model is thus based upon the principle of spatial heterogeneity. It concerns organisms whose interactions with each other during some part of their life history take place within small local populations. Wilson called such local populations "trait groups," defined as the subpopulation within which the actual ecological interactions take place. Trait groups are typically much smaller than their containing demes. Mosquito larvae occupying a pool of water in a pitcher plant, for example, interact among themselves, but are effectively isolated from the larvae in other pitchers. Bark beetles excavating galleries in a tree likewise have frequent interactions with each other, but have little or no interaction with the bark beetles laboring in other trees. Trait group isolation is not, however, a permanent situation. Many species undergo an annual dispersal phase in which individuals leave their trait groups and mix into the global population to mate. Mating in the global population is essentially random with respect to previous trait group membership. After mating, individuals (or their offspring) form new trait groups, and the cycle begins again.

Wilson invites his readers to consider how gene frequencies in the global population or deme might be affected by this cycle of within-trait group interaction and dispersal into the global population. In particular,

Notice that unlike Wynne-Edwards' model of group selection, Wilson's model does not require that individuals forego immediate gains in fitness for the sake of the long-term benefit of the group. By helping others the altruist is also helping himself. Wilson calls such behaviour "weak altruism," to distinguish it from "strong altruism" according to which aiding others involves a net sacrifice of fitness on the part of the actor. On Wilson's model the benefits for a trait group arising from an individual's actions are shared by the actor as well. He considers the emphasis on strong altruism in the form of spectacular displays of self-sacrifice on the part of individuals, and the difficulty of explaining how this can evolve, to be the chief impediments to taking group selection seriously. By focusing instead on behaviors which are individually as well as group advantageous, he suggests, "natural selection on the level of populations, or group selection" can be set on a firmer theoretical foundation.

Maynard Smith's Critique of Wilson's Intrademic Group Selection Model

Group selection, it seemed, had enjoyed a remarkable reversal of fortune. By the mid-1980s group selection had once again entered the mainstream, such that Wilson could cite one reviewer's observation that "decent folk can once again discuss it as a viable mechanism". [9] These new models, however, gave rise to a second round of controversy. The "neo-group selection controversy," as I shall call it, concerned less the biological plausibility of the models than the question of whether the processes described by these models were correctly described as group selection.

Maynard Smith argued that there are two essential requirements for calling a process "group selection," and that Wilson's model fails both. First, "For group selection, the division into groups which are partially isolated from one another is an essential feature". (As Wilson himself acknowledged, treating trait groups as discrete groups simply makes the mathematics easier, and is not essential to his model.) Second, according to Maynard Smith, "The term group selection should be confined to cases in which ... groups be able to "reproduce," by splitting or by sending out propagules, and that groups should go extinct". Neither of these processes, Maynard Smith held, characterize Wilson's trait groups. [11] Consequently, although Wilson has described a process which is both possible and may occur in nature, it should not be designated as "group selection". On Maynard Smith's view, Wilson's model is best understood as one in which "interactions occur between non-relatives," and is thus "best regarded as a form of individual selection" of the kind known as frequency-dependent selection. [12] The term "group selection" was already in use to refer to the models of Wright and Wynne-Edwards, and the application of this term to the quite different process Wilson proposed can only result, Maynard Smith argued, in widespread confusion. Wilson, on the other hand, asked "Is the structured deme model a form of group selection? .... It would be a pity to avoid calling it group selection simply because that term has been applied to a different conception of groups in the past...". [13]

What is remarkable about this disagreement is that although Maynard Smith and Wilson apparently agree about the nature of the processes themselves, they disagree about whether such processes are rightly designated as "group selection". Is the process Wilson describes really distinct from those individual level selection processes usually analyzed using the notion of inclusive fitness? Models of both types of processes have as their central assumption that populations are "viscous," i.e., that individuals do not have equal chances of interacting with all other members of the population with respect to genetic similarity, and that interactions may affect an individual's realized (inclusive) fitness. Maynard Smith argued that Wilson's model is insufficiently distinct from the ideas of frequency-dependent selection and inclusive fitness to justify classifying it as a different kind of model. Wilson disagreed, and has argued vigorously in recent years that the process described by his model is distinctive enough from individual selection to merit the appellation "group selection". [14] The controversy over neo-group selectionism rages on, and shows little sign of abating any time soon. [15]

Conclusion

It should be clear from the foregoing review that the question of "group selectionism" is not solely an empirical matter of observing or collecting data about biological systems. The debate over group selection has always concerned fundamental questions about how to subdivide natural systems into biologically meaningful entities, the extent to which assumptions made for the sake of mathematical tractability represent biologically realistic conditions, and questions about how to weigh historical precedent in describing various processes in nature. It is this multi-faceted character of the question of "group selection" that has made the debate over it so persistent, and promises to sustain its controversial status well into the next century.

References

[1] Darwin, C.R. The Origin of Species. John Murray, London, 1859.

[2] Ruse, M. Annals of Science 37, 615-630, 1980.

[3] Wynne-Edwards, V.C. Animal Dispersion in Relation to Social Behaviour, Oliver & Boyd, Edinburgh, 1962.

[4] Allee, W.C. et al. Principles of Animal Ecology, W.B. Saunders Co., Philadelphia, 1949.

[5] Provine, W. Studies in the History of Biology 2, 167-192, 1978.

[6] Maynard Smith, J. Nature 201, 1145-1147, 1964.

[7] Lack, D. Nature 203, 98-99, 1964.

[8] Williams, G.C. Adaptation and Natural Selection, Princeton University Press, Princeton, 1966.

[9] Wilson, D.S. Annual Review of Ecology and Systematics 14, 159-188, 1983.

[10] Wilson, D.S. The Natural Selection of Populations and Communities, Benjamin/Cummings, Menlo Park, CA, 1980.

[11] Maynard Smith, J. Quarterly Review of Biology 51, 277-283, 1976.

[12] Maynard Smith, J. In Current Problems in Sociobiology (ed King's College Sociobiology Group), 29-44. Cambridge
        University Press, Cambridge, 1982.

[13] Wilson, D.S. American Naturalist 113, 606-610, 1979.

[14] Wilson, D.S. American Naturalist (Supplement) 150, 112-125, 1997.

[15] Levin, R. Natural History 105, 12-17, 1996.
 

Figure 3 Lack's theory of population regulation differed from that of Wynne-Edwards in fundamental respects. Whereas Wynne-Edwards believed that groups actively regulate population numbers by adjusting the birth-rate in response to resource availability, Lack held that individual organisms engage in an unregulated ("scramble") competition for limited resources, and that population numbers are limited by the availability of such resources.

                                                                              Theories of Population Regulation

                                                                Lack's Theory                    Wynne-Edwards's Theory

Ultimate factors limiting population growth	Food shortage, predation, disease, climate	Capacity of habitat to yield sustainable food supply
Proximate factors limiting population growth	Environmentally-induced mortality; species-specific resource-modulated reproduction	Access to socially regulated distributions of conventional goods
Immediate objects  of competition	Limited "natural" resources: food, mates, space (e.g., breeding sites)	Conventional tokens: territories, social status (i.e., dominance)
Type of competition	"Scramble": unregulated competition for limited resources	"Tournament": regulated distribution via competition for conventional tokens
Explanation of resource-modulated reproduction	Optimization of individual fitness benefits	Contribution to population fitness benefits
Primary and secondary objects of natural selection	(1) Organisms (2) Genes	(1) Social Groups  (2) Organisms