If you’ve read the critiques of the Nowak et al. paper on kin selection that I highlighted this morning, you may have noticed a conspicuous absence among the authors: the name of Richard Dawkins.  Why, as the most famous exponent of kin selection since W. D. Hamilton, didn’t he co-author one of the critiques?

It turns out that nobody asked him.  I think this was simply an oversight, because all of us simply assumed that Richard would be penning his own criticism.  He didn’t, but he did write a brief piece on Nowak et al. for New Scientist, which he decided not to publish.  I’m posting it here with his permission, along with a link to his excellent paper about common misunderstandings of kin selection.  I’m not sure whether Richard will answer comments from readers, but you can certainly pose them below. Here’s his take on Nowak et al.:

This is no surprise. Edward Wilson was misunderstanding kin selection as far back as  Sociobiology, where he treated it as a subset of group selection (Misunderstanding Two of my ‘Twelve Misunderstandings of Kin Selection‘: Zeitschrift für Tierpsychologie 1969). Kin selection is not a subset of group selection, it is a logical consequence of gene selection. And gene selection is ‘standard natural selection’ theory. Inclusive fitness theory is not some kind of supernumerary excrescence, to be ‘resorted to’ only if  ‘standard natural selection theory’ is found wanting (Misunderstanding One). On the contrary, inclusive fitness theory is one way of expressing what was logically inherent in the neo-Darwinian synthesis ever since the 1930s but had been largely overlooked because people didn’t think hard enough about collateral kin. ‘Standard natural selection theory’ MINUS inclusive fitness would be like Euclidean geometry minus Pythagoras’ theorem.

Another way of expressing what was logicially inherent in the synthesis is Hamilton’s rule, rB>C: a gene for altruism will spread if the cost to the altruist, C is exceeded by the Benefit to the recipient, B, devalued by the coefficient of Relatedness, r. If you think, as Nowak et al. do, that ‘Hamilton’s rule almost never holds’, that simply means you haven’t been measuring B and C carefully enough. r is not the only term in Hamilton’s inequality. B and C matter too, and your game theoretic considerations are subsumed within them.

Perhaps most irritating is Nowak et al.’s concentration on haplodiploidy, which, in Hamilton’s original paper was a throwaway side-issue, interesting enough to pique the interest of generations of students, but not in any sense central to his paper. Of course Hamilton was well aware that eusociality is present in diplo-diploid animals, exactly as inclusive fitness theory would predict given appropriate B/C ratios. Indeed, Hamilton himself put forward an ingenious theory of the evolution of eusociality in termites, predating by seven years the version usually attributed to Bartz (attributed by Hamilton himself, indeed, with characteristically absent-minded generosity as I described in The Selfish Gene, second edition p 317).

Finally, Nowak et al. do Darwin an injustice, in discussing his theory of the evolution of worker sterility in social insects. They paraphrase Darwin’s ‘well-flavoured vegetable’ analogy. Let me quote it exactly: “Thus, a well-flavoured vegetable is cooked, and the individual is destroyed; but the horticulturalist sows seeds of the same stock, and confidently expects to get nearly the same variety . . . I do not doubt that a breed of cattle, always yielding oxen with extraordinarily long horns, could be slowly formed by carefully watching which individual bulls and cows, when matched, produced oxen with the longest horns; and yet no one ox could ever have propagated its kind. Thus I believe it has been with social insects . . .” It is true that Darwin goes on to phrase his idea in terms of benefit to the colony, but his analogy of the long-horned (castrated) oxen could not be clearer. No colony is involved. This is early inclusive fitness theory. It is entirely clear that, if Darwin had been alive to read Hamilton on social insects, he would have embraced inclusive fitness, not as an add-on to natural selection theory but as the logical way to express it in the age of the gene.

Last August I wrote about a new paper in Nature by three Harvard biologists, Martin Nowak, Corina Tarnita, and Edward O. Wilson.   Their paper was, as I called it, a “misguided attack on kin selection,” referring to the form of selection in which the reproductive success of a gene (usually a gene that affects behavior) is influenced not only by its effects on its carrier, but also by its effects on related individuals (kin) carrying the same gene.  This idea, introduced to evolutionary biology by George Price and W. D. Hamilton, has been enormously productive, explaining all sorts of things from parental care and parent-offspring conflict to sex ratios in animals and, perhaps most important, the evolution of “altruism.”  Nowak et al.’s paper attacked the idea that this form of selection—based on a gene’s “inclusive fitness”—was important in explaining anything; indeed, they didn’t even see kin selection as a form of natural selection.  My original post details most of my objections to their paper.

Now, seven months later, Nature has published a spate of objections to the Nowak et al paper: there are five critiques and a response to them by Nowak et al.  Here are the papers and links:

“Inclusive fitness theory and eusociality” by Patrick Abbot et al.  I am an author on this paper, along with one hundred and thirty six other authors.  The list of authors and their institutions, which occupies two pages of the three-page letter, reads like a Who’s Who of social evolution.  It’s telling that nearly every major figure in the field lined up against Nowak et al.

“Only full-sibling families evolved eusociality” by Jacobus J. Boomsma et al.

“Kin selection and eusociality” by Joan E. Strassmann, Robert E. Page, Jr., Gene E. Robinson and Thomas D. Seeley, four big names in social insect evolution

“Inclusive fitness in evolution” by Regis Ferriere and Richard E. Michod

“In defence of inclusive fitness theory” by Edward Allen Herre and William T. Wcislo

and the reply, called simply

“Nowak et al. reply“

I won’t go through the critiques, but their main points are these:

• Nowak et al.’s insistence that there’s a difference between inclusive fitness theory and “standard natural selection” theory is simply wrong.  The former is just a special case of the latter taking into account the effects of a gene in one body on the effects of other bodies also carrying that gene.  As Ferriere and Michod note:

“In fact, there is only one paradigm: natural selection driven by interactions, interactions of all kinds and at all levels. Inclusive fitness has been a powerful force in the development of this paradigm and is likely to have a continued role in the evolutionary theory of behaviour interactions.”

• Nowak et al.’s insistence that kin selection theory requires a number of restrictive assumptions that makes it largely invalid is also wrong.
• Nowak et al.’s insistence that the idea of kin selection has been of no value in in understanding nature is wrong.  Our own paper gives many examples in which kin selection theory has clarified or advanced our understanding of phenomena like eusociality in insects (the phenomenon of an insect colony that contains a cast of nonreproductive individuals), sex ratio, altruism spite, alarm-calling, and so on.  Further, the idea of kin selection has led to testable predictions—predictions that have been verified.
• Nowak et al.’s own “new” theory for explaining eusociality becomes a disguised form of kin selection when it tries to explain eusociality.

Curiously, in their very short reply, Nowak et al. don’t really address the criticisms, but merely reiterate what they said in their original article.  They resort instead to legalisms, explaining away the success of kin selection theory by saying this:

Abbot et al.claim that inclusive fitness theory has been tested in a large number of biological contexts, but in our opinion this is not the case. We do not know of a single study where an exact inclusive fitness calculation was performed for an animal population and where the results of this calculation were empirically evaluated.

This is a misunderstanding of how kin selection theory—indeed, all of evolutionary theory—is used. You don’t have to perform an “exact inclusive fitness calculation” to make predictions. (It’s nearly impossible anyway to “exactly” measure fitness in nature under any form of selection!)  In sex ratio theory, for example, one can predict that if a female wasp is the only individual parasitizing a fly pupa, and all offspring wasps mate within the pupa, then you need produce only enough males to fertilize all your daughters, producing a female-biased sex ratio.  But if more than one unrelated wasp parasitizes that pupa, you must invest in more sons to compete with the other wasps’ sons in fertilizing females, and so your relative production of males should increase.  That prediction has been amply verified without “exact” fitness calculations.  (Indeed, insofar as quantitative predictions can be made, they’ve fit the data remarkably well.)

In his piece on the kerfuffle, Carl Zimmer also noticed the non-responsive nature of Nowak et al.:

Nowak et al respond to all the criticism and don’t budge in their own stand. They claim that their critics have misinterpreted their own argument. And they claim that sex allocation does not require inclusive fitness. Oddly, though, they never explain why it doesn’t, despite the thousands of papers that have been published on inclusive fitness and sex allocation. They don’t even cite a paper that explains why.

If the Nowak et al. paper is so bad, why was it published? That’s obvious, and is an object lesson in the sociology of science.  If Joe Schmo et al. from Buggerall State University had submitted such a misguided paper to Nature, it would have been rejected within an hour (yes, Nature sometimes does that with online submissions!).  The only reason this paper was published is because it has two big-name authors, Nowak and Wilson, hailing from Mother Harvard.  That, and the fact that such a contrarian paper, flying in the face of accepted evolutionary theory, was bound to cause controversy.  Well, Nature got its controversy but lost its intellectual integrity, becoming something of a scientific National Enquirer. Oh, and boo to the Templeton Foundation, who funded the whole Nowak et al. mess and highlighted the paper on their website.

The lesson: if you’re a famous biologist you can get away with publishing dreck.   So much for our objective search for truth—a search that’s not supposed to depend on authors’ fame and authority.  I feel sorry for co-author Corina Tarita, a young scientist with splendid qualifications, for this paper will always cast a shadow over her career.