Saturday, August 28, 2010

Why EO Wilson’s Latest Eusociality Paper Fails

Martin Nowak, Corina Tarnita and E.O. Wilson made the cover of Nature this week with their article “The evolution of eusociality.” The argument presented in the paper is that inclusive fitness theory is an extraneous, unnecessary concept that has failed to provide insights into the evolution of eusociality.

Here are a few of the reasons why I think that their argument fails:

Failure 1: In the first couple of paragraphs, the paper guides unwary readers into accepting two false premises; the first is that kin selection and inclusive fitness are alternatives to “standard natural selection theory,” and the second false premise is that altruism is synonymous with eusociality.

Explanation: The authors confuse altruism (one type of cooperative behavior) with eusociality. Eusociality is a type of social organization seen in bees, ants, termites, naked mole rats, and a variety of other critters. The sophisticated level of cooperation exhibited by these groups can be achieved through a host of mechanisms; including mutualisms, rewarding, active enforcement, policing, reciprocity and a number of other phenotypes. Altruism is just one mechanism for cooperation; explaining altruism isn’t the same as thing as explaining all of eusociality, and explaining eusociality doesn’t explain all altruism. Despite the authors’ intended objective of detailing the evolution of eusociality (a long term process), they continuously revert to explaining only short term altruistic behavior – these are not the same thing.

The distinctions between kin selection, inclusive fitness, and “standard natural selection theory” are discussed in Failure 2 below.

Failure 2: Under the heading “Rise and fall of inclusive fitness theory” on page one of the paper the authors incorrectly/narrowly define both kin selection and inclusive fitness.

Explanation: The authors write, “The defining feature of kin selection theory is the concept of inclusive fitness…”

No it isn’t. The idea of inclusive fitness is central to modern biology and refers to the combination of both direct fitness (i.e. the reproductive success of the individual) AND indirect fitness (e.g. an individual controlling or manipulating other reproducers in proximity). Kin selection represents only a limited portion of inclusive fitness; more specifically, it’s a subset of indirect fitness.

Kin selection is the sort of cooperative behavior in which an organism works to enhance the reproductive success of a relative. (By helping relatives, organisms can increase the percentage of their family’s genes in the larger population.) In contrast to kin selection, inclusive fitness is the measure of an individual’s total ability to affect the passing of its genes to the larger gene pool. Inclusive fitness exists even in the complete absence of relatives and kin selection. More broadly, inclusive fitness can even be viewed as the modern interpretation of Darwin’s original linkage between adaptation and differential survival and can thus be seen as wholly coinciding with natural selection.

Failure 3: The authors make the “Selfish gene assumption”

Explanation: Immediately following Failure 2 described above, the authors enter into a discussion as to the validity of Hamilton’s rule (Relatedness >cost/benefit). The gist of their argument here is that because there are in existence eusocial animals with a low degree of familial relationship (e.g. those with diplodiploid sex determination) Hamilton’s rule is not valid. I call this failure the “Selfish gene assumption” because I’ve heard the same erroneous interpretation made during critiques of Richard Dawkins’ book the “Selfish Gene.”

Some folks incorrectly assume that Richard Dawkins forwards a view in which a single copy of a gene – a single gene in a specific individual – unintentionally works to be passed on to future generations. This isn’t the case. The book the “Selfish Gene” describes a perspective in which all genes for a specific phenotype – all copies present in the entire population - unintentionally work to increase in frequency. This may seem like a subtle difference, but it isn’t. It isn’t a subtle difference because like Dawkins in the Selfish Gene, Hamilton expressed relatedness in terms of genetic frequency, not in terms of genealogical proximity. Therefore, if E.O. Wilson and the other authors of the currently evaluated paper want to 'disprove' Hamilton, they shouldn’t be so concerned with the degree of familial relatedness shared between two INDIVIDUALS; rather, they should be concerned with the frequency of one individual’s genes as compared to the population’s gene pool as a whole. It doesn’t matter if individuals in a group are sisters, brother and sister, or third cousins twice removed – what does matter is genetic similarity. Members of a group can hold a huge compliment of genes in common without having the same parents.


Getting a bit lengthy, so I’ll stop here for now; the three “failures” listed above can be found on the first two pages of the paper. Rather than moving on to page three, I’ll wrap-up by saying that in the paper’s conclusion the authors summarize the stages of natural selection they believe to be required for the evolution of eusociality. This may not come as a surprise, but all of the listed stages could be explained in terms of inclusive fitness...

In summary, the paper doesn’t offer anything novel and in my opinion represents merely the latest pitch for group selection view - a pitch that fails on page one due to lack of a shared vocabulary.

Nowak, M., Tarnita, C., & Wilson, E. (2010). The evolution of eusociality Nature, 466 (7310), 1057-1062 DOI: 10.1038/nature09205


  1. Not too lengthy, I'd be interested in your thoughts on the rest of the paper! I read it yesterday, and either a) I'm an ignoramus, or b) they are at a tangent to my understanding of evolution. I just don't get what they are trying to argue, nor really understand where they get their premises from. But it is in Nature, so it must be good, and I must be able to understand it!

  2. Interesting. I don't remember where I saw it (because the question is large and tangential to my usual interests) but I recently saw a listing between group selection and kin selection/inclusive fitness, that IIRC came to the same conclusion as here. I.e. roughly: group selection concepts are explainable by inclusive fitness (but it doesn't explain all what the inclusive fitness mechanisms does).

    Well, _that_ and this was interesting, I'm trying to steer clear from the contested areas here. (Not a biologist.)

  3. Hi Johnny.
    Amazing that the learned editors of Nature, and their reviewers, didn't spot these points! Or perhaps you don't really understand the issues, which is sadly evident from this post.

  4. eleanor: Thanks for the comment. I’m sure that neither you, nor the authors of the eusociality paper are ignoramuses – there just seems to be a language barrier of sorts. And it’s not that I think that the group selection view is ‘wrong’ per se, it’s just that to me it just doesn’t seem very informative. Thanks again!

    Torbjörn: Thanks for the comment; I agree that it’s a fascinating area of study. The views expressed above certainly didn’t originate with me; they’re just based on my understanding of the subject. Thanks!

    starcourse: Thanks for the comment. I’m certainly not opposed to being corrected; where am I gong wrong? [For the sake of my comprehension, if you should opt to offer corrections please keep them in the realm of science; I have little interest in enduring the pseudoscience and creationist nonsense that you’ve placed on other sites.]

  5. And there is another issue about this paper. It ostensibly got into Nature as something called "Analysis" without peer review. But the supplement is actually a 43 page piece of mathematical analysis which mixes up typical Nowak formalism with all sorts of editorial asides.

    Can we say that Wilson and Nowak are free-riders?

    Besides Nowak's formal argument was made more elegantly and cogently nearly a year ago by van Veelen, Journal of Theoretical Biology 259(2009)589–600

  6. Nature's sensationalist editorial policy as of late is a very good argument for not caring about impact factors.

  7. Paul – it does seem a bit peculiar. Thanks for the comment!

    Gunner – Got to make a living I suppose…. Thanks for the comment!

  8. The points made in the paper are old ones. There is no new contribution to the theory of evolution. It simply argues he doesn't like (as even he calls it) the accounting technique often made in kin selection arguments. The main simplification he objects to (arbitrarily small mutations in phenotype space) is standard for any tool to study adaptation (unlike dynamics, which is Nowak's usual emphasis).

    It is important to understand what the paper is and what it's not. It gathers together objections that he and others have made over the past couple decades, with no new arguments. Most 'kin selection theorists' already know the assumptions in the current approaches and in disagreement with Nowak, are very happy with the power of the method. The most annoying part is that eusociality is a pretense to smuggle in a 50 page critique on inclusive fitness tools, very little of which even mentions his model.

  9. Paul: Of course it had a full peer review. It is called "analysis" because it is much more substantial than a normal article.

    Anon: if it really were "no new contribution" why did it make the cover of Nature. Nature just doesn't publish junk. I can only assume you don't understand the paper properly or the maths. Kin selection theorists are "happy with the power of the method" but that says more about their mathematical comfort zones than about scientific reality.

  10. starcourse: you tell me what's new in the paper, so I can refer you to papers making the same points years before. The objections of inclusive fitness analysis are well-documented; in fact Nowak has been making them for a while now. In terms of eusociality, Wilson has been saying this for years. What's billed as new in the model which combines the two is that queens have full choice of offspring traits (never mind that there is much conflict within colonies); this idea is also not new.

    In recent years, Nature has become sensationalist. Look up their article last year entitled "A nail in the coffin for group selection" for a pro-kin selection slam against group selection. This argument is for some reason very heated, and Nature editors know it'll get attention.

    "It is called 'analysis' because it is much more substantial than a normal article." You just made that up. It is called analysis because it is not a proper research article, and though it was indeed peer reviewed, the review process was much less stringent than for an a normal research article. What other "very substantial" papers in the history of the journal, had this "analysis" label?

    "I can only assume you don't understand the paper properly or the maths"... then please explain it to me, or respond on substance.

  11. Sorry you didn't read the full paper. If you do you might realize that at least theoritically inclusive fitness theory is not necessary to explain eusociality. Aultruism becomes a meaningless concept in this theoretical framework.