The haystack model (see T&R VIII) includes many assumptions but one was especially biased. Recall that each haystack is colonized by a single fertilized female bearing four genes coding for docility or aggressiveness--two of her own and two from her mate. Maynard Smith assumed that if even one of these genes codes for aggressiveness, then the aggressive gene entirely replaces the docile gene by the time the mice disperse from the haystack. The docile gene is not just at a selective disadvantage within groups. It is as disadvantageous as it can possibly be.
Hamilton's theory, which Maynard Smith dubbed kin selection, made a different set of assumptions. Hamilton modeled altruism as an interaction between two individuals. Like the good Samaritan helping someone in need, an altruist increases the fitness of the recipient by an amount b and decreases its own fitness by an amount c. Selfish individuals happily receive but do not give.
Since Maynard Smith was trying to compare kin selection with group selection, it seems only fair to use Hamilton's definition of altruism in the haystack model. This can be easily done. As before, we assume that haystacks are colonized by a single fertilized female, only now the genes code for altruism and selfishness as defined by Hamilton. Within each group containing both genes, the selfish gene has the advantage and starts to replace the altruistic gene. The rate that this happens depends upon the particular values of the b and c terms. For example, if a group is initiated by one altruistic and three selfish genes, and if the mice disperse after ten generations, then the altruistic gene might decline from an initial frequency of 25% to a frequency of 8%, but there is no reason why it must necessarily decline to zero.
Similarly, groups that start with more altruistic genes grow faster than groups starting with more selfish genes, and the rate that this happens depends upon the particular values of the b and c terms. For example, after ten generations, groups initiated by one altruistic and three selfish genes might be 40% more productive than groups initiated by four selfish genes.
The modified haystack model captures the essence of what I call the original problem (see T&R II), just like the original haystack model. In both cases, the trait that is "for the good of the group" is selectively disadvantageous within groups and requires a process of between-group selection to evolve. In the modified model, however, the b's and c's are allowed to determine the relative importance of within- and between-group selection, rather than arbitrarily assuming that within-group selection is as strong as it can possibly be.
What is the result of the modified haystack model? It turns out that altruism can evolve by group selection, using reasonable values of b and c, even when the altruistic gene is initially rare in the total population. The model that led to the rejection of group selection is favorable for group selection after all.
What was the impact of the modified model? Did it cause the entire field to reconsider the rejection of group selection? Not in the least. Nobody even thought to modify the original model until 1986, when I published an article titled "The haystack model revisited" in the journal Evolution. By then, group selection was thoroughly taboo and the article had no noticeable impact.
It gets worse. In 1970, George Price published a model that divided evolution into within- and between-group components and clearly indicated a role for between-group selection. The Price equation is regarded as a thing of beauty by theoretical biologists today, but at the time it had virtually no impact on the triumphant march of individual selection theory that had begun only a few years earlier. In 1975, Hamilton reformulated his theory on the basis of the Price equation, as I will recount in a future installment. According to Hamilton's new interpretation, kin selection is a kind of group selection rather than an alternative to group selection. During the same year, I published my first model demonstrating the plausibility of group selection--but the individual selection bandwagon rolled on.
So much for blustery claims by Dawkins in 1982 and Alexander in 1987 that the search for plausible models of group selection had been exhausted. When we focus on the original problem, there is near universal agreement among theoretical biologists that between-group selection can successfully counter within-group selection. The recent Nature article on group selection (see T&R VII) quotes the theoretical biologist Andy Gardner as saying "Everyone agrees that group selection occurs."
The fact that Gardner remains one of the most severe critics of multilevel selection theory will be explained in a future installment. Moreover, his statement accurately applies only to theoretical biologists knowledgeable about the subject. The vast majority of evolutionists receive their knowledge of theory secondhand, starting from textbooks when they are students. For them, the claim that group selection remains theoretically unsupported still rolls on. The situation is even worse for people from other fields interested in evolution and for the general public, who receive their knowledge of theory third, fourth and fifth hand.
The events that I have recounted provide a fascinating example of stasis in science, whereby a major decision becomes set in stone and is not easily revised, even when it richly deserves to be. If they knew then what we know now, group selection would never have been rejected as theoretically implausible. Yet, the field as a whole does not spontaneously clean up its mess after the fact. That is why a deliberate effort is required. Andy Gardner and I might disagree at some level, but I think I speak for both of us when I say that group selection is theoretically well supported. That should be the new consensus view. Those who disagree should familiarize themselves with the current literature before repeating the formulaic statements of the past.