Richard Dawkins (1) begins his review of E.O. Wilson's (2) new book The Social Conquest of Earth with an appeal to authority--namely the 137 evolutionists who co-authored a reply (3) to an article by Martin Nowak, Corina Tarnita and Wilson in Nature magazine (4). Appealing to authority is a risky business in science, as Dawkins appreciates, because scientific progress often involves the few prevailing against the many. Nevertheless, Dawkins' appeal to authority acknowledges something that everyone should know about group selection, kin selection, and all that: Dawkins and Wilson are only two of dozens of scientists who have been working on the issues over a period of decades. This is in contrast to their outsized images on the public stage, as if they are the only two figures meriting attention and all the important ideas sprang from them.
I mean Dawkins and Wilson no disrespect by calling them two among many. I trust that they would agree and would defer to others especially when it comes to mathematical models, which is not their area of expertise. If the public is going to become literate on the issues at stake--as well they should, because they are fundamental to the study of human sociality--then they will need to realize that both Wilson and Dawkins get some things right and other things wrong. Moreover, the entire community of scientists is in more agreement than the infamous exchange in Nature seems to indicate. Taking the argument from authority seriously can lead to a breakthrough in the public's understanding of social evolution.
Wilson has written abundantly on his rejection of kin selection in favor of group selection, as he thinks of it. Dawkins' review is the first time he has written at length on the topics of group and kin selection in many years, as opposed to little snippets here and there. I will therefore use Dawkins' review to outline the zone of consensus that exists among the many, which both Dawkins and Wilson should abide by unless they provide compelling arguments and evidence to the contrary.
The Origin of Group Selection and Kin Selection Theory
The seeds of both group selection theory and kin selection theory are present in the work of Charles Darwin, and both were invoked to address a single problem--how traits that are "for the good of the group" can evolve when they are selectively disadvantageous within groups. Examples include the sterile castes of bees and the human moral virtues. As one answer, Darwin proposed that groups of individuals who behave for the good of their group would outcompete other groups, even if their solid-citizen behaviors were selectively disadvantageous within groups. This was the seed of group selection theory. Darwin invoked it repeatedly in the corpus of his work, as Elliott Sober (5) has documented in detail. Dawkins is wrong when he asserts that Darwin invoked group selection in only "one anomalous passage"; he needs to read and refute Sober's article or acknowledge his own error on this relatively minor point.
As another answer, Darwin used the analogy of animal and plant breeders selecting traits that involve sacrificing individuals by breeding their relatives, which was the seed of kin selection theory. It is unclear whether Darwin regarded these as different or equivalent explanations, nor does it matter for anything but historical interest.
In the received history that just about everyone agrees upon, many biologists during the first half of the 20th century assumed that adaptations evolve at all levels of the biological hierarchy, including individuals, social groups, species, and ecosystems. Either there was no awareness that group selection might be necessary, or it was assumed that between-group selection would be strong enough to oppose within-group selection. Today this position is known as naïve group selectionism. It came under intense scrutiny in the 1960's and a consensus emerged that while between-group selection is possible in principle, it is almost invariably weak compared to within-group selection in nature. If behaviors evolve that appear to be "for the good of the group", then they must be explained without invoking group selection. All of the other theories for explaining the evolution of cooperative and altruistic social behaviors, such as kin selection, reciprocity, and selfish gene theory, were explicitly developed as alternatives to group selection.
As an influential example that is also described by Dawkins in his review, John Maynard Smith constructed a simple mathematical model in which mice live in haystacks for a number of generations before dispersing to colonize a new set of haystacks. The mice vary in their aggressiveness. Aggressive mice beat docile mice within haystacks, but groups of docile mice are more productive than groups of aggressive mice. The haystack model corresponds exactly to what Darwin described in words. Maynard Smith concluded on the basis of his model that the between-group advantage of docility was insufficient to counter the within-group advantage of aggressiveness. If docility exists in nature, it would need to be explained another way, such as W.D. Hamilton's newly minted theory of kin selection--a term coined by Maynard Smith, which Hamilton called inclusive fitness theory.
Everything I have said so far falls within the zone of consensus of the many, including Dawkins and Wilson. I would be surprised if anyone knowledgeable about the subject disagreed with it, and I encourage them to speak up if they exist.
On Replicators and Vehicles
George C. Williams in Adaptation and Natural Selection (6), followed by Richard Dawkins in The Selfish Gene (7), articulated the concept of genes as replicators. According to their argument, sexually reproducing individuals are unique combinations of genes that will never reoccur and therefore do not qualify as units of selection. A unit of selection must replicate with high fidelity and only genes have this property.
Individual organisms don't qualify as replicators, but they remain important as vehicles of selection, which explains their functional organization. A vehicle is a collection of genes that survive and reproduce as a unit. In an analogy made famous by Dawkins, vehicles are like rowers on a crew team that can only win the race by pulling together. Genes do occasionally evolve to succeed at the expense of other genes within the same organism, such as cancer and meiotic drive, but they are relatively uncommon and tend to undermine the functionality of the organism when they occur.
Williams borrowed the replicator concept from population genetics theory, where it is known as "average effects"--the fitness of alternative genes, averaged across all contexts. It is an important concept for many purposes, but it says nothing about group selection. Group selection models always posited genes for altruism (favored by between-group selection) and selfishness (favored by within-group selection). Whenever between-group selection prevails against within-group selection (however rarely or implausibly) the altruistic gene has the highest average effect and evolves in the total population.
A lot of confusion existed on this point, especially since calling genes the "fundamental unit of selection", based on their status as replicators, made it seem as if this constituted an argument against group selection. By now the dust has fully settled, however. Everyone, including Dawkins in his review, agrees that if selfish gene theory has anything to say about group selection, it must involve something other than the concept of genes as replicators.
The only other major concept articulated by selfish gene theory is the vehicle. The paradigmatic vehicle is the individual organism, which provides very few options for genes to succeed other than as part of the collective. But here we encounter a problem: Recall Maynard Smith's model, in which the groups are populations of mice living in haystacks. These groups are nothing like individual organisms. There is nothing restricting aggressive mice from outcompeting docile mice within the groups. Nevertheless, if the between-group advantage of docility was sufficient to counter the within-group advantage of aggressiveness, then it would count as an example of group selection. Nothing more organism-like would be required of the groups. When we survey other models and verbal descriptions of group selection prior to the advent of selfish gene theory, the assumptions about groups vary in their details, but all of them are mere collections of individuals in which altruistic traits are selectively disadvantageous but nevertheless can potentially evolve on the strength of the differential contribution of the groups to the total population. Organism-like properties of the groups were never required.
Thus, if we define the vehicle concept too narrowly in reference to individual organisms, then it fails to represent what has always been understood by group selection. Either selfish gene theory is inadequate for studying group selection, or the vehicle concept must be broadened to include the groups that have always been posited in group selection models.
As an aside, both high-fidelity replicators and individual organisms as airtight vehicles are products of evolution, which means that they are not required for the process of evolution to take place. The original argument that sexually reproducing individuals don't qualify as replicators failed to identify single phenotypic traits as candidate replicators. Socrates might never come again as a large collection of traits, but the shape of his nose or aspects of his intellect might reoccur with the same frequency generation after generation. As long as the phenotypic distribution of a trait is replicated and responds to selection, high-fidelity replicators are unnecessary. The concept of "evolution without replicators" is required not only to describe evolution before the advent of genetic replicators (8), but aspects of ongoing cultural evolution (9).
The Advent of Equivalence
A watershed event took place in the 1970's, when W.D. Hamilton encountered the work of George Price, which has been ably chronicled by Oren Harman in his book The Price of Altruism (10). Price developed an equation that partitioned selection in the total population into within- and between-group components. It was like Maynard Smith's haystack model in concept, but much more general, and it showed that between-group selection could plausibly prevail against within-group selection. Moreover, when Hamilton translated his own inclusive fitness theory in terms of the Price equation, he realized that altruism expressed among kin is selectively disadvantageous within kin groups and evolves only by virtue of the differential contribution of kin groups to the total population. In other words, inclusive fitness theory was not an alternative to multilevel selection theory but included the elements of multilevel selection within its own structure. The reason this was not obvious before is because Hamilton's method of calculating the net effect of an altruistic gene on copies of itself predicted whether it would evolve in the total population, but did not reveal its local selective disadvantage and the corresponding need for between group selection to evolve.
Other theoretical models published during the 1970's and 80's, including my own trait-group model (11), Michael Gilpin's model that was the first to incorporate nonlinear interactions (12), and my re-analysis of Maynard Smith's haystack model (13), showed that the wholesale rejection of between-group selection as a significant evolutionary force was just plain wrong. Hamilton's realization for inclusive fitness theory goes for all evolutionary theories of social behavior, regardless of what they are called. All assume that social interactions take place in groups that are small compared to the total population. The traits labeled cooperative and altruistic typically are selectively disadvantageous within the groups and require the differential productivity of groups to evolve in the total population. This is expressed in the Price equation as a negative within-group term and a positive between-group term that sums to a net positive average effect for the altruistic trait. The Price equation can accommodate many kinds of groups, including those that have always been the province of group selection models.
The Price equation also helped Hamilton realize that his original interpretation of r, which was largely restricted to genealogical relatedness, could be generalized to include any correlation between the genes of the donor and genes of the recipient(s), for any reason. Moreover, Hamilton's original formulation remained useful for calculating what evolves in the total population, even if it didn't partition selection into within- and between-group components along the way. The choice of which framework to use became largely a matter of preference, with any given result from one framework translatable into the other framework.
Thus was born the era of pluralism and equivalence in sociobiology. It has become part of the zone of consensus of the many, but Wilson and Dawkins are not among them. Both fail to recognize that the era of "kin selection vs. group selection" has passed. Most of the important questions can be asked within either framework and can be translated between frameworks.
What prompted the 137 co-authors to respond to the Nature article was not based on what Nowak et al. said about group selection, but their denial that it could also be framed in terms of inclusive fitness theory or that ideas framed in terms of inclusive fitness theory had ever proven to be useful.
Holding Dawkins Accountable
Curiously, while the many have spoken against Wilson's outdated views about kin selection, they remain largely silent on Dawkins' outdated views about group selection. I will therefore list points made by Dawkins in his review (in italics) that have been rejected by the many long ago. Dawkins can argue on their behalf if he likes, but he cannot invoke the argument from authority.
1) "Group selection: the poorly defined and incoherent view that evolution is driven by the differential survival of whole groups of organisms." Multilevel selection theory is defined as coherently as inclusive fitness theory.
2) "The American grey squirrel is driving our native red squirrel to extinction..." Choosing an example of competitive exclusion between species to illustrate group selection is poorly informed. Even the concept of species selection, which is different than the concept of group selection within species, is not represented by competitive exclusion (14).
3) "So biologists with non-analytic minds warm to multilevel selection..." Multilevel selection models are just as analytic as inclusive fitness models. In fact, proponents of inclusive fitness theory often praise it as more intuitive than multilevel selection theory. As an aside, accusing those who disagree with you of mental weakness is unbecoming to a scientist.
4) "With the exception of one anomalous passage in The Descent of Man..." As previously mentioned, Darwin articulated the concept of group selection numerous times in the full corpus of his work. If Dawkins wishes to claim otherwise, he should respond to the detailed scholarship of Sober. Historical revisionism is unbecoming to a scientist.
5) "Genes are the primary replicators, organisms are the obvious vehicles, but what about groups? As with organisms, they are certainly not replicators, but are they vehicles? If so, might we make a plausible case for 'group selection'? This passage is followed by a list of examples involving huddling penguins, hunting lions, birds in flocks, fish in schools, racing cyclists, and hens in flocks. In most of these examples, the basic problem of cooperation and selfishness arises. Whenever the traits that maximize relative fitness within groups are not the same as the traits that maximize collective benefits, between-group selection is required to counteract within-group selection. Groups do not need to be organism-like in any other respect, as previously explained. Using inclusive fitness theory to study the same examples does not change any of the facts concerning within- and between-group selection.
6) "Convincing examples are vanishingly hard to find." There is abundant empirical evidence for between-group selection, including extensive experimental evidence (15). Hens in flocks provide a compelling example, in which aggressiveness is favored within groups and docility between groups, just like Maynard Smith's haystack model (16). The reader is invited to type "group selection" and "multilevel selection" into Google Scholar to consult both the theoretical and empirical literature.
7) "[Wilson] treated kin selection as a special case of group selection, an error that I was later to highlight in my paper on "Twelve Misunderstandings of Kin Selection." Wilson was right to conceptualize kin selection as a special case of group selection during the 1970's, which was consistent with Hamilton's interpretation based on the Price Equation. Since then, inclusive fitness theory has been generalized to the point where it is equivalent to multilevel selection rather than a special case. Maynard Smith's haystack model, for example, which he created to distinguish group selection from kin selection, can easily be seen as an example of kin selection.
8) "Bert Hölldobler (yet another world expert who will have no truck with group selection)..." Dawkins should consult with people before making such assertions. Hölldobler disagrees with Wilson's strong rejection of kin selection but is perfectly receptive to group selection and understands the principle of equivalence. He represents what I have been calling the consensus of the many when he states (personal communication, cited with permission): "Almost everyone agrees that selection can also operate on the level of the colony. Indeed a colony can serve as a vehicle of genes, and one can model this by employing inclusive fitness theory or multilevel selection theory."
Recovering the Important Questions
Dawkins is so intent on preserving his views on group selection that his review of Wilson's book does not describe the main thesis of the book. Wilson claims that we are a eusocial species (which he defines in terms of cooperation and not reproductive division of labor), the primate equivalent of the eusocial insects, which accounts for our dominance of the earth. Mark Pagel advances the same thesis in his book Wired for Culture (17), which he frames in terms of selfish gene theory, calling human cultures vehicles of selection. The groups that serve as vehicles (as Pagel would put it) or targets of selection (as Wilson would put it) are not composed of close genealogical relatives. Heritable phenotypic variation among groups is achieved in different ways, such as norms enforced by punishment. Similar mechanisms suppress self-serving behaviors within groups, so that the balance between levels of selection tilts heavily in favor of between-group selection. It doesn't matter that the same basic thesis can be framed in terms of multilevel selection theory, selfish gene theory, or inclusive fitness theory. It remains new and important either way.
Other issues that were originally framed in terms of group selection vs. kin selection remain important, despite the fact that they now can be addressed within either framework. Take the role of genealogical relatedness in the evolution of insect eusociality. When Wilson observes that species with high r values are common while the evolution of eusociality is rare, he is saying that high r values are not sufficient to explain the evolution of eusociality and might not even be necessary. Modest r values might be sufficient and there are even sensible models that work with very low r values. All of these possibilities can be framed in terms of inclusive fitness theory and Wilson is wrong to claim otherwise--but the issues remain interesting and important either way. If we overlook what Wilson says about kin selection, what he says about group selection deserves our attention.
Taking the Argument from Authority Seriously
In this article, I have described Richard Dawkins and E.O. Wilson as two among many who have been studying kin selection and group selection over a period of decades. I also have claimed that there is a zone of consensus of the many and that both Dawkins and Wilson are outliers who fail to recognize that the days of pitting kin selection against group selection are over.
Dawkins invoked the argument from authority to criticize Wilson's position and to support his own. If my analysis is correct, then both Dawkins and Wilson should bring their views into alignment with the many or at least stop invoking the argument from authority to support their own views. Of course, it is possible that I have misrepresented the consensus of the many. If so, then I'm sure that many will be willing to correct my own errors.
This article first appeared on Evolution: This View of Life
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2. Wilson, E. O. (2012). The Social Conquest of Earth. New York: Norton.
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12. Gilpin, M. E. (1975). The theory of group selection in predator-prey communities. Princeton, NJ: Princeton University Press.
13. Wilson, D. S. (1987). Altruism in mendellian populations derived from kin groups: the haystack model revisited. Evolution, 41, 1059-1070.
14. Jablonski, D. (2008). Species Selection: Theory and Data. Annual Review of Ecology and Systematics, 39, 501-524.
15. Goodnight, C. J., & Stevens, L. (1997). Experimental studies of group selection: What do they tell us about group selection in nature? American Naturalist, 150, S59-S79.
16. Muir, W. M., Wade, M. J., Bijma, P., & Ester, E. D. (2010). Group selection and social evolution in domesticated chickens. Evolutionary Applications, 3, 453-465.
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