Some ideas are born and raised within the realms of biology and later put to rest, either because they no longer fit the paradigm or they are disproven so strongly that they have no chance of survival. The idea of group selection should be put to rest for neither of these reasons. It has been surgically altered so many times that its contributions to biology are no longer visible. This is not to say that group selection should never have been discussed; this discussion has resulted in a much clearer vision of the process by which natural selection operates. Indeed, its legacy lives on in other ideas such as species selection and clade selection.
However, the idea of group selection has recently become too problematic. Begun in the '60's by V.C. Wynne-Edwards, the idea was started as an argument "for the good of the species" (Wynne-Edwards, 1962) G.C. Williams responded with an emphasis on a genetic perspective of natural selection in opposition to the idea of group selection. The rebuttal in favor of group selection has been from two schools of thought. One is an offshoot of Wright's shifting balance theory, in which mathematical and experimental models of group selection have been attempted. The other is a theoretical perspective that historically stems from Wynne-Edwards' initial ideas. These ideas have not been well accepted for valid reasons to be discussed later; thus group selection cannot offer us a working model for natural selection.
The idea must be put to rest, but its soul should live on. Biology should work towards observing interactions between organisms that do not yield personal gain at the expense of another as an immediate reward; as D.S. Wilson stated it,
"Again and again, treatments of biological communities pay passing tribute to 'complex interrelationships among species' and then lapse into food webs and competition models as if nothing else existed." (Wilson, 1980)
Thus, the traditional emphasis on natural selection in the form of competition has underscored other relationships between animals that also influence their survival. Some examples of these are, "Plants form 'defensive guilds,' protecting each other from predation", and "Fish ectoparasites are decreased by activities of cleaning fish." (Wilson, 1980) The idea of group selection has raised an issue that must be addressed in biology: that higher levels of interactions between organisms, groups, and species must be emphasized in biological thought. Watching nature shows on television only supports the notion that organisms are traditionally viewed in a simplistic manner; and these impressions come directly from today's scientific biases. However, reductionistic black-and-white ideas about the genetic side of natural selection are not sufficient to explain why colorful ecosystems evolve and function the way they do.
II. BIRTH OF THE IDEA
In 1962, V.C. Wynne-Edwards introduced the idea of group selection to bring the discussion of natural selection to a new level that had traditionally been de-emphasized by biologists.
"There are a great many important characters... that are in the nature of collective attributes, all possessing the common quality of contributing the welfare and survival of the group... and when necessary subordinating the interests of the individual." (Wynne-Edwards, 1962)
Thus came the idea of group selection as a process in which an individual acted for the good of the group, regardless of whether it should benefit the individual or be detrimental to the individual. Though some will debate that the motivation behind this concept resulted from 1960's discourse about peace and cooperation, Wynne-Edwards raised a much deeper conflict that stemmed from the theory of natural selection and its applications in biology: neo-Darwinian natural selection overemphasized a reductionistic perspective about animal behavior without considering the contributions of higher levels of interactions between organisms.
III. ADOLESCENCE
G.C. Williams again raised the topic of group selection for debate in Adaptation and Natural Selection (Williams, 1966). Unfortunately, "naive group selectionist" (Wilson and Sober, 1994) biologists such as Wynne-Edwards were making assumptions that group selection was a valid phenomenon; yet the theory was without concrete justification. (Problems with Wynne-Edwards' reasoning will be discussed later). Chapter four put the debate into perspective: organismal adaptations were a result of either genic selection (individual selection or organic selection) or group selection (biotic selection). If all the individuals in a population reduced their rate of reproduction because of limited food resources, one could argue either way. Either the individuals reduced their reproductive rate so that the entire population could survive and flourish (group selection); or each individual reduced their reproductive rate to avoid its own death, revealing inherently selfish behavior (genic selection). Through framing the argument as such, Williams diametrically opposed the two processes of selection; thus I will call it the extremist argument. He brought up a good discussion on group selection and clearly organized the topic; however, his definition of group selection strictly limited its possibilities through the expectation that any adaptation attributed to group selection could not have a component of individual selection.
Williams asserted that "only the gene is stable enough to be effectively selected", thus leaving individual selection as the more important rule. He also introduced a way to prove the process of group selection on an empirical level:
"Our search must be specifically directed at finding adaptations that promote group survival but are clearly neutral or detrimental to individual reproductive survival in within-group competition." (Williams, 1966)
According to Williams, a researcher must prove that group selection is at work only by default: in cases where individual selection or genic selection is definitely not at work. This criterion makes logical sense in that one must disprove all other possible scenarios before proving the existence of group selection. However, it is so narrow that it becomes almost impossible to achieve experimentally. In addition, it underscores the more philosophical underpinnings of group selection. According to Williams' narrow definition of natural selection (at the level of the gene), we forget that individuals do live in groups and that they constantly interact with other organisms throughout their short life spans. The extremist argument is raised time and time again in discussions of group selection, and it constitutes the biggest criticism of any group selection theory. Although Williams presents a false dichotomy in the extremist argument against group selection, there is no way of circumventing the narrow definition it assumes. This criticism of the extremist argument (i.e. that it is too narrow) is by no means direct proof that group selection is an important phenomenon in evolution. It does, however, raise the issue that individual selection should incorporate phenomena that occur at the group level or higher.
IV. ADULTHOOD
From here, most biologists were convinced that group selection was not worthy of their time. Since then, the topic has experienced a resurgence of interest from various different perspectives. These may be grouped into either empirical/experimental categories and theoretical/philosophical categories (though these are not mutually exclusive). Whereas empirical studies have focused primarily on the level of subpopulations so that genetic correlations would be possible to analyze, theoretical analyses have expanded the discussion above and beyond the level of subpopulations, all the way up to clade selection. Though some arguments are more convincing than others, all of this work suggests that natural selection cannot be reduced to the level of genic selection alone.
V. EMPIRICAL/EXPERIMENTAL PERSPECTIVES
Sewall Wright developed the shifting balance theory to support a hypothesis about the evolution of sexual species (Wright, 1931), and Wade has since done extensive work on flour beetles in an attempt to demonstrate this theory (see Wade and Goodnight, 1991). These successful experiments have introduced the possibility of group selection under specific circumstances: namely, that of genetic differentiation between demes and differential gene flow, resulting in possible "happy gene combination[s]" (Crow, 1991) that exhibit group phenotypes rather than individual characteristics. According to Wade, group selection is the "process of genetic change which is caused by the differential extinction or proliferation of groups of organisms." (Wade, 1978)
Wade's experiments were ground-breaking in that they demonstrated a clear principle through empirical data that could be used to support group selection. Through the differential dispersion of demes according to relative fitness, a set of demes could overcome the problem of stasis on separate adaptive peaks. Over time, gene flow would allow less fit demes to move from lower adaptive peaks to higher ones, thus increasing the overall fitness of the group (as a collection of demes). Thus, Wade argues that group fitness has increased through selection at the group level: by way of higher-level interactions between individual organisms. Because genetic documentation for the process was achieved through an analysis of genetic variance between populations, the Wright process became more than simply a model. Wade brought interest back into the idea of higher-level selection. Selection was supposedly acting at the group level, and Wade demonstrated that it occurred through a genetic component.
Still, Wade had not convinced the extremists that the Wright process demonstrated group selection, although he did show that the Wright process worked. The most serious conceptual problem raised with Wade's experiments as proof of group selection has been, once again, that his data could be reinterpreted as proof of individual or genic selection. Wade himself described this as the Fisherian viewpoint:
"... the ultimate fate of a gene is determined by its average effect with respect to fitness within large populations and that co-dependent gene complexes arise largely as a by-product of the effects of selection on single genes." (Wade, 1991)
Thus, we return to the same problem Williams introduced to the group selection debate: that even though group selection was possible, individual selection was also possible, with a "sorting" (Gould and Vrba, 1986) effect at the level of the group. I cannot offer an answer to this dichotomy; I can only offer my perspective on the situation from a broader perspective. To some extent, whether the Wright process demonstrates group selection or individual selection is irrelevant. Through his experiments with flour beetles, Wade proved that the Wright process can work; and he also provided genetic documentation for the process. It would be more productive if biologists concentrated on the process rather than disputing over units of selection.
Advocates of Wright and Wade have more recently used contextual analysis as an empirical model to meld the two concepts of individual and group selection together. Contextual analysis looks at scenarios in which natural selection may be divided into both individual and contextual components. For example, multilevel selection is "variation in the fitness of individuals that is due to both properties of the individuals and properties of the group or groups of which they are members." (Goodnight et al, 1992) Though my understanding of mathematics is not sophisticated enough to understand how they actually achieve this, the ideas which motivate the number-pushing are long past due. Rather than taking an easy route and explaining selection through genes only, these thinkers have once again begun with the understanding that organisms and genes form complex levels of interactions, all of which affect the framework of the process of evolution.
VI. THEORETICAL/PHILOSOPHICAL PERSPECTIVES
These perspectives are largely based upon logical conjectures about organisms, and increasingly less upon factual data. Though the ideas are often expressed without supporting examples that use real-world situations, they benefit the discussion in that they are the driving force towards the models in which to test hypotheses about group selection.
Wynne-Edwards can be accredited for developing the concept initially from a natural history perspective. The entire 601 pages of Animal Dispersion in Relation to Social Behaviour discusses higher level interactions between organisms; much of this is then related to fitness and group selection:
"... socialisation is a general phenomenon, which from comparatively lowly and obscure beginnings has undergone progressive evolution, so that in the more advanced groups it has tended to become increasingly more conspicuous and complex." (Wynne-Edwards, 1962)
Despite his unjustified belief that asocial organisms are primitive and "lowly", Wynne-Edwards made it clear that evolutionary biologists could not ignore social organization in their theories about evolution. He makes similar claims today; and the positive aspect of his treatment of group selection is that he always discusses his hypothesis within a natural history framework. In more recent work on the red grouse, Wynne-Edwards reasserts his theory on group selection in terms of food abundance. More simply put, "each individual is normally programmed through its genetic code to take a part in maintaining the balance of nature", through keeping track of the current food supply and altering its behavior such that the whole group will survive. (Wynne-Edwards, 1991)
The problem with this analysis is that he makes grand, general, unsupported claims when he addresses the controversy about group selection. For example, in developing the argument that gene pools evolve rather than individuals, he claims that mortality is an adaptation, the result of which generates "an endless supply of new genotypes, all of them (except identical twins) different from one another." (Wynne-Edwards, 1991) In addition, he makes logical jumps from one assumption to the next: he denies the neo-Darwinian emphasis on individual selection by assuming that organisms would inevitably engage in a "ruthless pursuit of self-advantage and prolific fecundity," should this be true. Wynne-Edwards makes the same mistake as Williams did in his extremist argument: he radically opposes group selection and individual selection, and then takes sides without justification. Though Wynne-Edwards does support his theory with real-life examples, he has no support from controlled studies that make convincing arguments in his own favor.
Recall that contextual analysis was one method to dissolve the extremist argument using multilevel selection, in selection involving both group and individual characteristics could act simultaneously. D.S. Wilson has made a similar accomplishment in dissolving the extremist argument within his theoretical model of group selection. For example, he has shown that group selection and altruism are not equivalent concepts:
"Between-group selection is required for the evolution of both weak and strong altruism, but the degree of altruism cannot be used as an index for the importance of between-group selection in the evolution of a trait." (Wilson, 1990)
Though he agrees that altruism and selection are related, he makes the distinction between strong and weak altruism, and asserts that strong altruism is not correlated with group selection. The primary difference between these two concepts deals with motivation: strong altruism is sacrificial behavior on the part of the individual being sacrificed (i.e. suicide), and weak altruism is sacrificial behavior on an organism by other members of the group. (Wilson, 1980, 1990) In his assertion that weak altruism may be correlated with group selection rather than strong altruism, he develops the possibility that a weakly altruistic behavior can evolve.
"To be consistent, one must either define group selection as that component of natural selection that operates on the differential productivity of local populations within a global system, or abandon the term altogether. There is already a trend toward renaming all forms of altruism that can evolve as 'genetic selfishness,' which presumably reserves the term 'altruism' for anything that can't evolve (Alexander 1974). This conceptualization is a hollow victory for the individual selectionist." (Wilson, 1980)
If altruism by definition implies that the behavior cannot evolve and the only way to prove the existence of group selection is through altruistic behavior, the idea of group selection becomes impossible. Thus, Wilson asserts that group selection should not be defined in terms of altruism, and weak altruism should be distinguished from strong altruism. In doing so, he restructures the debate that was formulated by Williams so that he no longer must take sides on either extreme. Yet once again, we must ask whether Wilson is able to restructure the debate. In his attempt to reconcile individual and group selection, he defines weak altruism as a trait that seems by definition competitive.
Wilson bases his argument for group selection in an analogy between groups and the concept of "superorganisms". This concept is a 'frameshifted' view of a group, in which each individual represents an organ within the group, whereas the group represents the organism. Through this analogy, he makes it easier to conceptualize selection acting upon a single entity (the superorganism), with both direct effects (superorganism survival) and indirect effects (such as beneficial environmental modification) resulting from this selection. (Wilson, 1980) Wilson and Sober have more recently formulated an argument for group selection from a reinterpretation of Dawkins' concepts of vehicles and replicators, much to the dismay of Dawkins. They define group selection as a process of natural selection that is effective only at the group level, in which social groups are 'vehicles' of selection. Analogous to Dawkins' view that individuals are vehicles that carry replicators without consistency (i.e. their genomes are blasted to smithereens), groups can be vehicles of replicators (genes) as well. (Wilson and Sober, 1994)
Dawkins rightfully encourages them to "bury the vehicle" (Dawkins, 1994), but he does so for the wrong reason. He asserts that vehicles are irrelevant to the central issue of replicators (genes), and that "There did not have to be any vehicles at all." In doing so, he returns to Williams' initial extremist argument, that genic selection is much more important than group selection. Once again, I cannot offer an answer to this problem. Yet the situation should be analyzed for what knowledge it can achieve about the process of evolution. Dawkins is once again skirting the reason why group selection was introduced to begin with: to gain a better understanding of higher levels of interactions between organisms and their subsequent influences on selection. The vehicle should be buried because it has crashed and burned too many times, but the some of the ideas which it represents should continue to influence biology.
VII. THE JOURNEY TOWARDS DEATH
Group selection has had a vibrant history. Wynne-Edwards raised the idea to propose that individuals may act against their personal benefit for the benefit of their groups. Though this line of reasoning was ill-founded, other schools of thought developed to discuss group-level interactions of organisms that had previously been ignored. These schools have also been limited in their ability to convince the scientific community of their validity, primarily because of the never ending argument that Williams presented twenty years ago. Nonetheless, their intentions are worthy of exploration; the scientific community should be pressured to incorporate group-level interactions into their studies.
It would be wrong to claim that biologists do not study higher levels of interactions among organisms; there has in fact been much work in these areas. For example, studies on multispecies coevolution and evolutionary arms races look at how dependency between organisms has affected their evolutionary pathways. (Linhart, 1991; Mitter et al, 1991) My point is that in light of the process (i.e. how associations affect fitness and survival of organisms), whether selection occurs on the individual or the group becomes irrelevant.
Try this new line of thought for a moment: what if we dropped the idea of group selection and instead discussed interaction selection? This would be a study of how the interactions between two or more individuals, between two or more groups, or between two or more species resulted in differential fitnesses of organisms or genes. In discussing interaction selection, we would transcend strict essentialist concepts such as individual selection and group selection, and reach a more pure form of analysis in which the process is emphasized rather than the unit of selection.
Despite its possible uses in sociobiology (which is too much to discuss in this paper; see Wilson and Sober, 1994) the idea of group selection is on its way out. Nevertheless, it has given us the basis for a more progressive attitude in the biological sciences, and has led us toward models of interactions between and among organisms. Group selection should remain in our history books as the founder of a new line of thought in biology, and go no further.
Literature Cited:
DAWKINS, R. 1994. Burying the Vehicle. Behavioral and Brain Sciences 17: 616-617.
GOODNIGHT, C.J., J.M. SCHWARTZ, and L. STEVENS. 1992. Contextual analysis of Models of Group Selection, Soft Selection, Hard Selection, and the Evolution of Altruism. American Naturalist 140:743-761.
LINHART, Y.B. 1991. Disease, Parasitism and Herbivory: Multidimensional Challenges in Plant Evolution. Trends in Ecology and Evolution 6:392-396.
MITTER, C., B. FARRELL, and D.J. FUTUYMA. 1991. Phylogenetic Studies of Insect-Plant Interactions: Insights into the Genesis of Diversity. Trends in Ecology and Evolution 6:290-293.
WADE, M.J. 1978. A Critical Review of the Models of Group Selection. The Quarterly Review of Biology 53:101-114.
WADE, M.J., and C.J. GOODNIGHT. 1991. Wright's Shifting Balance Theory: and Experimental Study. Science 253:1015-1018.
WILLIAMS, G.C. 1966. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press. Princeton, New Jersey. 307pp.
WILSON, D.S. 1980. The Natural Selection of Populations &;Communities. The Benjamin/Cummings Publishing Company, Inc. Menlo Park, California. 186pp.
______ 1990. Weak Altruism, Strong Group Selection. Oikos 59:135-140.
WILSON, D.S. and E. SOBER. 1994. Reintroducing Group Selection to the Human Behavioral Sciences. Behavioral and Brain Sciences 17:585-608.
WYNNE-EDWARDS, V.C. 1962. Animal Dispersion in Relation to Social Behaviour. Hafner Publishing Company. New York, NY. 653 pp.
______ 1991. Ecology Denies Neo-Darwinism. The Ecologist 21:136-141.
VRBA, E.S., and GOULD, S.J. 1986. The Hierarchical Expansion of Sorting and Selection: Sorting and Selection Cannot be Equated. Paleobiology 12:217-228.