By the 1960's, evolutionary theory had settled into a comfortable paradigm called the Modern Synthesis. With other major issues apparently settled (go here for an update on the Modern Synthesis), the issue of group selection began to occupy center stage. George C. Williams was not the only critic and the great AEPPS were not their only foil (see T&RIII). Across the Atlantic, the Scottish biologist Vero C. Wynne-Edwards published an ambitious volume titled Animal Dispersion in Relation to Social Behavior (1962), which claimed that animal populations evolve to avoid overexploiting their resources. Wynne-Edwards was aware that such restraint was "for the good of the group" and might be vulnerable to less prudent behaviors within the group. Nevertheless, he thought that between-group selection easily trumped within-group selection and proceeded to interpret a vast array of social behaviors as adaptations to regulate population size. His book stimulated widespread debate and skepticism from prominent evolutionists such as David Lack and John Maynard Smith.
Another major event in the 1960's was William D. Hamilton's inclusive fitness theory, more widely known as kin selection theory, a term coined by Maynard Smith. Hamilton reasoned that a gene for altruism could evolve if it favored copies of itself in the bodies of other individuals. An identical twin is certain to have the same genes as oneself, a full sibling has a 50% probability, and so on. For an altruistic gene to have a net benefit, the cost to the altruist must be outweighed by the benefit to the recipient multiplied by the probability of sharing the same gene identical by descent. Here was a way to explain the evolution of altruism -- among genealogical relatives, at least -- without invoking group selection. Indeed, Maynard Smith coined the term "kin selection" to distinguish it from group selection in an article criticizing Wynne-Edwards.
Hamilton's theory had a remarkable corollary. Ants, bees, and wasps (but not termites) have a peculiar genetic system called haplo-diploidy, in which females are produced sexually and have two sets of genes but males are produced asexually and have one set of genes. A consequence of haplo-diploidy is that, when a female mates with a single male, her daughters have a 75% chance of sharing the same genes (because they all get the same genes from their father) rather than a 50% chance for diploid species. Thus, not only did Hamilton's theory explain the general phenomenon of altruism among genealogical relatives, but in the same stroke it seemed to explain the extreme altruism exhibited by ants, bees, and wasps on the basis of their extreme degree of relatedness (termites remained an unexplained exception to this rule).
When Williams published his book Adaptation and Natural Selection in 1966, it seemed to provide a synthesis for the subject of group selection, settling the issue in the same way that the modern synthesis settled other major issues in evolutionary theory. Williams attacked naïve group selectionism and forcefully asserted what Darwin, Fisher, Haldane and Wright already knew: Higher-level adaptations require a process of higher-level selection and tend to be undermined by selection at lower levels. Here is one of his canonical statements (p. 92-93):
It is universally conceded by those who have seriously concerned themselves with this problem that...group-related adaptations must be attributed to the natural selection of alternative groups of individuals and that the natural selection of alternative alleles within populations will be opposed to this development. I am in entire agreement with the reasoning behind this conclusion. Only by a theory of between-group selection could we achieve a scientific explanation of group-related adaptations.
Notice that Williams is affirming the basic logic of group selection theory, but then he went further in a continuation of the same passage:
However, I would question one of the premises on which the reasoning is based. Chapters 5 to 8 will be primarily a defense of the thesis that group-related adaptations do not, in fact, exist. A group in this discussion should be understood to mean something other than a family and to be composed of individuals that need not be closely related.
In other words, even though group-level adaptations can evolve in principle, Williams claimed that in reality between-group selection is almost invariably trumped by within-group selection. This empirical claim became known as the theory of individual selection. The final sentence about families left the door open for kin selection, a point to which we will return.
Adaptation and Natural Selection was widely praised as a resolution to the group selection controversy. For the rest of the 20th century, group selection was taught primarily as a way not to think about evolution. "For the good of the group" thinking was regarded as just plain wrong. Everything that evolved by natural selection was interpreted as a variety of self-interest.
To be continued.