Evolution for Everyone

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.


  1. #1 abb3w
    October 26, 2009

    I again suspect the root of the problem is in a careless resolution of the riddle of the Ship of Theseus, since the nature of self-interest depends on defining what one means by the “self” as a function of time.

  2. #2 Alice
    October 26, 2009

    Curiously, these posts that were originally made at Huff Post have been deleted from that site, along with the commentary attracted at the time – and also along with Dr. Wilson’s own responses to that commentary, some of which were “qualifiers” to the inferences that ought to be drawn from that post.
    What’s my point here? Just that I’m curiouser and curiouser about the integrity of the process.

  3. #3 David Sloan Wilson
    October 26, 2009

    To Alice: My HuffPost site is still fully functional. Go to http://www.huffingtonpost.com/david-sloan-wilson/#blogger_bio . It’s fine for you to insist on integrity. Once you decide that I’m not willfully concealing information, I look forward to engaging you on the ideas.

  4. #4 Alice
    October 26, 2009

    Mea culpa. I had looked for the Huff posts last week and they (or so it seemed) were gone. Clearly, I should have checked again this morning before commenting.

  5. #5 Guy
    October 26, 2009

    Hi David,

    I’m enjoying your blog. I am intrigued by your quote of Hamilton in your most recent post, where he wrote:

    “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.”

    The term “group selection” was so charged back then (and for decades to come) that Hamilton appears to be trying hard to find an explanation for altruism evolution that he could articulate without using the tarnished group-selection language. As we know, he essentially succeeded in avoiding the hot-button phrases; but this quote seems to suggest he knew kin selection was actually a kind of group selection all along. Families are one kind of group. They are a kind of group that tend to exhibit high frequencies of alleles that are rare in the overall population, so they are a natural for linking selection at the level of the gene with selection at the level of the group. Again, I think Hamilton was surreptitiously successful in achieving this.

  6. #6 David Sloan Wilson
    October 26, 2009

    To Guy: I can’t resist replying to your message in detail. First, this passage is by Williams, not Hamilton. In 1957, George and his wife Doris published an article titled “Natural Selection of Individually Harmful Social Adaptations Among Sibs with Special Reference to Social Insects (Evolution 11:32-39). It was explicitly a group selection model, based on a previous model by Sewall Wright in 1945 (Ecology 26:415-419), in which the groups were families. The “individually harmful” traits were selectively disadvantageous within groups, as their label suggests, but benefitted the group, as the label “social adaptations” suggests. The fact that the groups were families provided lots of genetic variation among groups, increasing the strength of group selection, even though the socially advantageous trait was declining in frequency within each and every family containing both types. In other words, Williams and Williams (1957) were proposing that altruism evolves in families by group selection.

    Hamilton was unaware of this article when he developed his theory of inclusive fitness. Don’t ask me why–history is full of vicissitudes such as this. I doubt very much that it was due to a lack of integrity. The rule that he derived states when a gene increases the absolute number of copies of itself (identical by descent) in the total population. It is not at all obvious from Hamilton’s rule that the altruistic gene is increasing the number of copies of the non-altruistic gene in its group even more and that all the ingredients of group selection are required for it to evolve in the total population–all of which was clear in the Williams and Williams model. Hamilton therefore concluded that his theory explained the evolution of altruism without invoking group selection.

    When George encountered Hamilton’s theory (I know because I have discussed this extensively with him) he was amazed by it and regarded his own model as dumb by comparison. He felt especially chagrined because his model had social insects in mind but assumed diploidy, missing the crucial insight that Hamilton had about the extra-high relatedness caused by haplo-diploidy. In any case, Williams’ caveat about family groups left the door open for his own model as much as Hamilton’s.

    It wasn’t until Hamilton started interacting with George Price in the early 1970′s that he fully realized that inclusive fitness theory invokes group selection, rather than providing an alternative to group selection, as I will relate in a future installment. Yet, he was delighted rather than disappointed, suggesting that he was never strongly prejudiced against group selection. If you wish more detail, read chapter 2 of my book Unto Others (with Elliott Sober), Hamilton’s pivotal paper in 1975 (cited in Unto Others) and Hamilton’s own account in his book The Narrow Roads of Geneland.