Big dust-up about kin selection

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.

57 Comments

  1. Sven DiMilo
    Posted March 24, 2011 at 5:34 am | Permalink

    Thanks very much for the linx & summary; I’m looking forward to digging in later.

    Quick question: Why would kin selection be invoked to explain parental care? That seems to me like an obvious product of straightahead direct-fitness-benefit natural selection.

    • Posted March 24, 2011 at 7:36 am | Permalink

      Sven DiMilo asks: “Quick question: Why would kin selection be invoked to explain parental care? That seems to me like an obvious product of straightahead direct-fitness-benefit natural selection.”

      That is is precisely the point. There is no such thing as ‘straitahead direct-fitness-benetit natural selection’. Or rather there is but it logically and necessarily INCLUDES kin selection. It is just that most people, until Hamilton, overlooked that logical necessity. Biologists in the field now understand the point, and will continue to do so notwithstanding Nowak et al’s crass attempt to set the field back forty years. Nature’s decision to publish their paper was, as Jerry suggests, a public disgrace.

      • Sven DiMilo
        Posted March 24, 2011 at 8:19 am | Permalink

        That’s certainly a point, and a good one (and of course I agree 100% with your comment, including, if that wasn’t clear before, your last sentence).

        But it wasn’t ‘precisely the‘ point that I was making. I know ‘biologists in the field’ and how they think about things, and they speak routinely of direct benefits and indirect benefits of social behaviors to inclusive fitness. Direct benefits are from individual reproductive success, indirect benefits are from (the additional fitness components of) kin selection. My point was that parental care seems to me direct, not indirect as Dr. Coyne implied in the OP:
        “[kin selection] has been enormously productive, explaining all sorts of things from parental care and parent-offspring conflict to sex ratios in animals”.

        • Posted March 24, 2011 at 8:40 am | Permalink

          You are still wrecked among heathen dreams.

          What you say is correct if you insist upon making the distinction between ‘direct’ and ‘indirect’ benefits. My point is that that is not a distinction we should be making.

          • Sven DiMilo
            Posted March 24, 2011 at 10:23 am | Permalink

            that is not a distinction we should be making

            Number one in your taxonomy of misunderstandings, I believe.
            Without disagreeing that kin selection is the more general prediction of gene-selection theory (and that parental care can therefore be viewed as a special case of kin-selection theory), that still seems like an oddly strong assertion.

            Surely whether the distinction should be made or not depends on the questions one is asking about evolution.
            We analyze various components of fitness–and the trade-offs among them–all the time: survival vs. fecundity, egg size vs. clutch size, current vs. future reproduction, etc. Sexual selection is another general prediction of gene-selection theory, I believe, yet we still speak routinely about mating success as an especially interesting component of natural selection, as well as distinguishing intra- from inter-sexual selection.
            Of course most of these are not mutually-exclusive dichotomies anyway. There are various different taxonomies of components of fitness possible, each potentially useful answering specific questions about specific systems.

            How is distinguishing the direct and indirect components of inclusive fitness any more problematic or unwise?

            For one thing, understanding the evolution of non-social-behavioral phenotypes is hardly ever going to require invoking indirect benefits anyway, not because we physiologists (e.g.)(or is that ‘heathens’?) regard kin selection as a superfluous or last-resort theory, but because it’s simply not usually among the relevant fitness-components for the phenotypes we study.

            For another thing, it’s just an interesting question to ask sometimes. Take helpers at the nest in cooperatively breeding birds. Why do they do it? The (indirect) benefits predicted by gene-selection theory from helping to raise successful siblings? Or are direct benefits accruing as well? Might the helper inherit the territory later and reproduce directly? Maybe they are even getting extra-pair copulations (males) or dumping eggs (females) and achieving real-time direct benefits from helping at this nest?

            I think we should continue to make the distinction when it is edifying or interesting to do so.
            *shrug*

            • Thanny
              Posted March 24, 2011 at 12:32 pm | Permalink

              I think I understand why you want to believe there’s a distinction, but there isn’t.

              Why? Because the parent is not the offspring in a sexually reproducing species. All offspring are kin, and genetically no different than siblings (assuming diploidy).

              The only real difference is that the nature of the relationship is generally more clear.

              And as has been discussed here and elsewhere, when it comes to haplodiploids, offspring are less related than siblings, which makes total nonsense of “direct” versus “indirect” selection, as you put it.

  2. NewEnglandBob
    Posted March 24, 2011 at 5:35 am | Permalink

    I am making a huge amount of popcorn and making sure the big monitor is working well and taking a front row seat to be able to enjoy the show that is happening.

    Nowak, Tarnita, and Wilson being refuted by 150+ of the heavies of evolutionary biology is like watching a car accident while driving past it. One can not help but stare.

    I can guess which side DS Wilson is on, but that car wreck is getting old.

  3. Sven DiMilo
    Posted March 24, 2011 at 5:43 am | Permalink

    I feel sorry for co-author Corina Tarita, a young scientist with splendid qualifications

    ?
    She seems to be a mathematician who has never published on biology without Nowak.
    Now a paper with EO Wilson (a biologist even mathematicians have heard of) in Nature (a scientific journal even mathematicians have heard of)?
    It probably won’t hurt her career a bit. Hey, the reply even goes on her CV as another Nature pub for the bean-counters.

  4. Posted March 24, 2011 at 5:48 am | Permalink

    There’s several misconceptions here.

    Nowak et al. are not disputing that relatedness and interactions between relatives are important for the evolutionary success of a gene. Their argument is against the mathematical formulation of inclusive fitness theory. Making IF calculations requires certain mathematical manipulations which are not possible in general. They only work if a number of assumptions hold, as detailed in the mathematical appendix to their original paper.

    Inclusive fitness can be a useful rule of thumb for making qualitative predictions. But mathematically, it’s not a good tool. Population genetics and evolutionary game theory are much better for deriving quantitative results.

    • whyevolutionistrue
      Posted March 24, 2011 at 5:57 am | Permalink

      Their argument is against inclusive fitness as a tool for understanding nature, not just its mathematical formulation. And, as the critiques show—and will become evident when two longer critiques are published soon—you’re just flat wrong in saying that those mathematical manipulations are “not possible in general” or work only if “a number of assumptions hold”. Did you read the third paragraph of Abbott et al.? I get the impression you didn’t read the critiques.

      And inclusive fitness IS population genetics! It’s not something different.

      • Posted March 24, 2011 at 6:56 am | Permalink

        I have indeed read each one of the critiques. The third paragraph of Abbott et al. refers to regression-based approaches (e.g. Queller 1992). These approaches are mathematically silly: they take what is already known and manipulate it into a form that is purported to show Hamilton’s rule at work. While this can always be done, it never yields new information or predictions. In order to make new predictions using inclusive fitness theory, strong assumptions are needed.

        And it is wrong to say “inclusive fitness theory IS population genetics”. Inclusive fitness theory is a specific set of tools which are sometimes used within population genetics. To quote from Nowak et al.’s letter:

        inclusive fitness theory is a proper subset of the standard theory and makes no independent predictions. Any effect of relatedness is fully captured by the standard approach.

        • Troy
          Posted March 24, 2011 at 10:13 am | Permalink

          Rubbish. Kin selection theory with the regression definition of relatedness follows directly from population genetics models. No strong (or weak) additional assumptions are needed whatsoever, and this has been known a long time.

          Nowak et al. haven’t done their homework and are simply ignorant about this.

          There’s a paper in press by Andy Gardner (Univ Oxford) et al. in the Journal of Evolutionary Biology which IMO succeeds beautifully in clarifying this once and for all. Contact Gardner for a copy if you like.

          • Posted March 24, 2011 at 10:33 am | Permalink

            You haven’t contradicted my claim. Yes, regression can be used to write a form of Hamilton’s rule once the outcome of evolution is already known.

            But can such an approach be used to generate quantitative predictions about what new traits may evolve in existing populations? No, not without additional assumptions.

            This is because there is interdependence between the social traits under consideration and the relatedness structure of the population. So in the equation BR>C, each of the terms depends on all the others. This equation is therefore useless for prediction. One cannot vary any subset of the parameters without changing all the others.

            • Troy
              Posted March 24, 2011 at 11:02 am | Permalink

              “Yes, regression can be used to write a form of Hamilton’s rule once the outcome of evolution is already known.”

              Also when the outcome is unknown.

              “But can such an approach be used to generate quantitative predictions about what new traits may evolve in existing populations? No, not without additional assumptions.”

              Incorrect. Additional assumptions are not necessary, although they may be helpful (e.g. weak selection). The reason is that kin selection models are equivalent to population genetic models.

              “This is because there is interdependence between the social traits under consideration and the relatedness structure of the population. So in the equation BR>C, each of the terms depends on all the others. This equation is therefore useless for prediction. One cannot vary any subset of the parameters without changing all the others.”

              Partially correct. But one can consider R, B and C as dependent on a underlying evolving trait value and solve for an equilibrium value. Predictions can be made and have been made and tested.

  5. Posted March 24, 2011 at 5:50 am | Permalink

    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!)

    I will go one stop further and assert that it is impossible to exactly measure inclusive fitness. I came up with the below thought experiment while chatting with Bjørn Østman. Don’t be too distracted by the use of the peacock; it arose during a conversation relating partially to sexual selection, so that was the convenient example.

    50,000 years ago, two peacock brothers were walking through some bushes near a mountain. One brother’s tail was slightly larger than the others. This caused him to get momentarily caught in the bushes, while his brother continued on unimpeded. At that moment, a landslide occurred which crushed the smaller-tailed brother, but spared the longer-tailed brother as the momentary delay prevented him from being in the path of the avalanche. He frees himself from the bushes and goes on to leave many offspring.

    So now do we have a 10^-10% contribution to the inclusive fitness of “long tail” owing to “prevents peacock from walking into avalanche”? If not, why not, without invoking teleologial reasoning?

    The best answer I can come up with is that there is an implicit assumption that, on average, for every peacock who is spared from walking into an avalanche by a momentary delay, there is another peacock who would have been spared if he hadn’t been delayed. But we can’t prove that assumption, and in any case even if we had, we would not expect the numbers to be precisely equal, just approximately equal — so if we wanted to do an “exact” calculation of fitness, we are still potential left with some negligible mathematical contribution to the fitness of a longer tail due to random events like walking into a landslide.

    This is an intentionally absurd example, but that’s exactly the point I am making: Even if it were practical to calculate inclusive fitness “exactly”, such a metric would be useless, because it merely tells you what has already happened. Any useful concept of fitness is by necessity an approximation, because it needs to exclude factors that we believe would cancel themselves out over a long enough period of time (like a long tail saving a peacock from an avalanche).

    It’s kind of like how I get uncomfortable when car insurance companies try to over-refine their risk estimations. If you overdo it, it defeats the point. The perfect risk assessment is this: If you don’t get in an accident, you get insurance for free; if you do get in an accident, your premium is exactly what the insurance company paid out for your accident. In other words, no insurance. Risk assessment in insurance is by necessity an approximation, because otherwise it’s useless. Same with fitness, in my opinion.

    • Posted March 24, 2011 at 7:05 am | Permalink

      True, in the natural world, fitness can never be measured exactly.

      But part of this disagreement is a difference in perspective. Nowak and Tarnita (and myself) are mathematicians at heart. We are all interested in biology, but we believe that precise mathematical models are of great use in understanding nature.

      If you have a mathematical model, you should analyze it using exact methods whenever possible. Very often, this cannot be done using inclusive fitness techniques. But it CAN be done using good mathematics.

      The bottom line is that inclusive fitness is a inexact and unwieldy as a mathematical tool. Better tools are available.

      • J.J.E.
        Posted March 24, 2011 at 10:15 am | Permalink

        And had Nowak et al. simply written a paper saying “better tools are available” it would have been published in JTB or TPB and people in the field likely would be digested and adopted it in time. But no, they sought to play the roles of “paradigm changers”. So they shat all over IF as if their proposition weren’t simply an elegant generalizationbut was rather a completely novel contradiction providing heretofore inaccessible insights into social evolution.

        • J.J.E.
          Posted March 24, 2011 at 10:38 am | Permalink

          Er, novel “contribution”. Damn Swype autocorrect.

      • Troy
        Posted March 24, 2011 at 10:22 am | Permalink

        “If you have a mathematical model, you should analyze it using exact methods whenever possible. Very often, this cannot be done using inclusive fitness techniques. But it CAN be done using good mathematics.”

        For example?

        • Posted March 24, 2011 at 2:31 pm | Permalink

          An example would be just about any model in which one’s fitness effects depend in a nonlinear fashion on the composition of types among one’s interactors.

          To quote Gardner, West, and Barton (2007):

          “The most powerful and
          simple approach to social evolutionary problems is to start with a method such as population genetics (including the multilocus approach), game theory, or direct-fitness maximization
          techniques. The results of these analyses can then
          be interpreted within the frameworks that Price’s theorem and Hamilton’s rule provide.”

          In other words, Hamilton’s rule/IF theory are usually not useful for calculating or predicting evolutionary dynamics. Their main use is for reinterpreting results that have been derived by other means.

          • Troy
            Posted March 25, 2011 at 5:00 pm | Permalink

            That’s simply not true. There are plenty of dynamic evolutionary models based on IF. I’ve published several of them.

            Like Nowak, you seem to be confused about “exact mathematical models”. Game theory models are static models, sometimes equipped with an artificial dynamic. It’s well known that population genetic models and game theory models are generally not consistent.

            Oh well. This is not really a forum for technical discussions.

            • cooperator
              Posted March 25, 2011 at 5:10 pm | Permalink

              Troy and/or Ben, is there a way to take this conversation elsewhere? I’m curious what you two are actually trying to say.

              I have not seen a kin selection model that was dynamical (the way I interpret the term, i.e., differential equations), and it is simply not true that game theory models must be static. They actually lend themselves quite nicely to dynamical analysis.

              • Posted March 26, 2011 at 6:01 am | Permalink

                Perhaps we could discuss this more productively over email. Troy, am I correct in assuming that you are Troy Day? If so, I am a big fan of some of your work. I think Taylor, Day, Wild (2007) is a rare but shining example of how inclusive fitness theory can be used well. I have a paper currently under review that borrows some ideas directly from your work.

                My opinion is that IF theory works well in limited settings. My beef is when theorists attempt to generalize it to all of natural selection. All such attempts that I have seen involve a bizarre kind of proof by redefinition of the terms involved.

  6. Diego
    Posted March 24, 2011 at 5:56 am | Permalink

    I have often felt in the past that the only reason a particular paper was published by Nature is that it went against the prevailing paradigm, even if the article would have been better as ripped up paper to line an eagle’s nest. Nature choosing controversy over integrity happens time and again and I am no longer surprised by it.

    • Sven DiMilo
      Posted March 24, 2011 at 6:00 am | Permalink

      *shrug*
      They’re selling adspace, after all.

    • Posted March 24, 2011 at 6:10 am | Permalink

      Nature choosing controversy over integrity happens time and again and I am no longer surprised by it.

      Does this suggest that controversy is “Naturally” selected for?

    • Dan
      Posted March 24, 2011 at 6:47 am | Permalink

      I’m no longer surprised by it but I am still routinely disgusted by it. I think Coyne is right that this paper would not have been published with different authors, which to my mind makes a strong argument for double blind peer review.

  7. Dr. I. Needtob Athe
    Posted March 24, 2011 at 6:31 am | Permalink

    “I am an author on this paper, along with [i]one hundred and thirty six other authors[/i]. 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.”

    I’m confident that you’re on the right side of this dispute, but still, that argument is uncomfortably reminiscent of an infamous book titled “Hundert Autoren gegen Einstein” (Hundred authors against Einstein)

    http://en.wikipedia.org/wiki/100_Authors_Against_Einstein#Hundred_authors_against_Einstein

    • whyevolutionistrue
      Posted March 24, 2011 at 6:34 am | Permalink

      Just because we’re numerous—and there are many authors working directly in the field of inclusive fitness—doesn’t mean that we’re wrong!
      :-)

  8. Helen Wise
    Posted March 24, 2011 at 6:43 am | Permalink

    I’ve gone back to your original postings, popped over to Prof. Dawkins’ house and read his posting about this, and visited other ancillary sites as they appealed and occurred, and have just generally spent an enjoyable hour or two with this reading–all to diffuse my frustration that the Nature articles are behind pay walls. (Even if they weren’t, I am probably short one or two of the mental bed springs necessary to completely comprehend the underlying science and/or math, anyway.)

    That said, and revisiting an earlier topic, I think I’m going with Nowak for the Templeton prize win.

    • Marella
      Posted March 24, 2011 at 6:07 pm | Permalink

      Interesting suggestion!

  9. yesmyliege
    Posted March 24, 2011 at 6:51 am | Permalink

    If this paper is as bad as described, then Templeton has really crossed the line from obnoxious to dangerous.

    Their pernicious influence, formerly relegated to fluffy opinion pieces, philosophy, and soft science, has now had a corrupting effect on one of the premier hard scientific resources of the reality-based world. Any scientist who now associates with them from this point forward is taking a huge risk with his reputation.

    And kudos to Dr Coyne for bravely spearheading the criticism of the malevolent Templeton.

  10. Kevin
    Posted March 24, 2011 at 7:12 am | Permalink

    There’s always the chance that this is plate tectonics. But the probability of that seems exceedingly low.

    I think Wilson’s status as eminence gris might be getting a little too gris. That he’s pulling a couple of other mathematical biologists along with him should be no surprise whatsoever.

    But from what I’ve read here (without checking the articles themselves — darn pay walls!), it appears that Nowak might be contradicting his earlier paper in Science. Nowak, M. (2006) Five Rules for the Evolution of Cooperation. Science 314, 1560.

    Anyone have access to that article who can check?

      • Kevin
        Posted March 24, 2011 at 1:47 pm | Permalink

        Looks to me like a fairly standard review article that does not in any way call into question the validity of kin selection as a part of the modern evolutionary model. In fact, he provides mathematical support for kin selection as a component of natural selection of altruistic behavior.

        Unless I’m reading this wrong and someone way more qualified than I am to comment tells me otherwise…it looks like this paper basically contradicts the current one.

        Not that there’s anything wrong with coming to a different conclusion based on new facts — but I’m still looking for the facts upon which the new conclusion was reached.

        • Posted March 24, 2011 at 5:25 pm | Permalink

          Let’s set one thing straight: Nowak’s beef is with the matheamtics of inclusive fitness theory, not with kin selection. He states this clearly in his brand-new general audience book “Supercooperators” (p. 110)

          You may think, given my somewhat withering analysis of inclusive fitness, that I think kin selection is dead. This is not the case. Despite its limitations, Hamilton’s rule has been a valuable heuristic… [But] the mathematical understanding of evolutionary dynamics has advanced to the point where the theory of sociobiology can be extended beyond Hamilton’s rule… Kin selection is still a mechanism for the evolution of cooperation, as long as it is properly defined.

    • J.J.E.
      Posted March 24, 2011 at 1:03 pm | Permalink

      In reading that, it does indeed appear that Nowak ca 2010 is contradicting Nowak ca 2006. I hasten to point out that there is nothing wrong with this. But just for fun, here are some interesting excerpts to that effect:

      When J. B. S. Haldane remarked, “I will jump into the river to save two brothers or eight cousins,” he anticipated what became later known as Hamilton’s rule (1). This ingenious idea is that natural selection can favor cooperation if the donor and the recipient of an altruistic act are genetic relatives. More precisely, Hamilton’s rule states that the coefficient of relatedness, r, must exceed the cost-to-benefit ratio of the altruistic act:

      r > c/b (1)

      Relatedness is defined as the probability of sharing a gene. The probability that two brothers share the same gene by descent is 1/2; the same probability for cousins is 1/8. Hamilton’s theory became widely known as “kin selection” or “inclusive fitness” (2–7). When evaluating the fitness of the behavior induced by a certain gene, it is important to include the behavior’s effect on kin who might carry the same gene. Therefore, the “extended phenotype” of cooperative behavior is the consequence of “selfish genes” (8, 9).

      Kin selection has led to mathematical theories (based on the Price equation) that are more general than just analyzing interactions between genetic relatives (4, 5). The interacting individuals can have any form of phenotypic correlation. Therefore, kin selection theory also provides an approach to compare different mechanisms for the evolution of cooperation (69, 70).

      References
      1. W. D. Hamilton, J. Theor. Biol. 7, 1 (1964).
      2. A. Grafen, in Oxford Surveys in Evolutionary Biology,
      vol. 2, R. Dawkins, M. Ridley, Eds. (Oxford Univ. Press,
      Oxford, 1985), pp. 28–89.
      3. P. D. Taylor, Evol. Ecol. 6, 352 (1992).
      4. D. C. Queller, Am. Nat. 139, 540 (1992).
      5. S. A. Frank, Foundations of Social Evolution (Princeton
      Univ. Press, Princeton, NJ, 1998).
      6. S. A. West, I. Pen, A. S. Griffin, Science 296, 72
      (2002).
      7. K. R. Foster, T. Wenseleers, F. L. W. Ratnieks, Trends Ecol.
      Evol. 21, 57 (2006).
      8. R. Dawkins, The Selfish Gene (Oxford Univ. Press, Oxford1976).
      9. E. O. Wilson, Sociobiology (Harvard Univ. Press,
      Cambridge, MA, 1975).

      69. L. Lehmann, L. Keller, J. Evol. Biol. 19, 1365 (2006).
      70. J. A. Fletcher, M. Zwick, Am. Nat. 168, 252 (2006).

      • Kevin
        Posted March 24, 2011 at 1:51 pm | Permalink

        Yep. Those are the money quotes — but seem to be just standard exegesis on what is kin selection. Later in the paper, he does a little mathematical voodoo and provides support for kin selection as a component of the evolution of altruism.

        Looks pretty uncontroversially in favor of kin selection to me. And cites Wilson in the process!

  11. cooperator
    Posted March 24, 2011 at 9:24 am | Permalink

    I think there are two separate issues at stake. The first is the usefulness of kin selection theory as an explanatory tool. The other is the usefulness of the mathematical models developed in the name of kin selection.

    From a philosophical point of view, kin selection is obviously a very useful explanatory tool. However, from a mathematical point of view, kin selection is a mess. That doesn’t mean it’s wrong – some things are intrinsically messy. Nowak attacked the mathematical models, stating (incorrectly, I think) that they are only valid in the “weak selection limit”. I think it’s more accurate to say that without that simplifying assumption the models would be even harder to formulate correctly. Suffice it to say that the mathematical models of kin selection are (by necessity) extremely oversimplified. For example, since they are (usually) based on the Price equation, there are no time dynamics in the models. What kind of model of change ignores time?! The kin selection modelers are aware of this, of course, but they seem to think it doesn’t matter.

    The problem with the kin selection partisans is that they think way to highly of their models. They believe they have shown that cooperation can only evolve by kin selection, and in particular that multi-level selection can be explained by kin selection. This is wrong, dead wrong. The Price equation has nothing to say about (true) multi-level selection because in the Price equation the number of groups has to be a constant quantity. (It can’t deal with group-level events.) The idea that the Price equation captures multi-level selection correctly is probably the fundamental misunderstanding in this whole “kin selection = group selection” debate. The two are not – I repeat – not the same.

    • Kevin
      Posted March 24, 2011 at 1:54 pm | Permalink

      If you read his 2006 Science paper (link provided above), he does not make that error. In fact, there are even graphics in the paper that demonstrate the difference between different proposed evolutionary mechanisms of altruism, including kin selection and group selection.

      Of course, I don’t have access to the new paper, so I can’t say whether he’s done any new math — but the critiques I’ve read of the paper imply that he has not.

      Curiouser and curiouser.

    • Torbjörn Larsson, OM
      Posted March 27, 2011 at 3:48 pm | Permalink

      What kind of model of change ignores time?!

      Game theory has been mentioned, I believe one of your comments mention that dynamics have to be imposed. The wavefunction of the universe comes to mind for a similar problem.

      Then famously there is general relativity, which as a geometric theory has to recapture time as some condition that splits the spacetime metric into space slices. (I think, not having studied GR.) “Each solution of Einstein’s equation encompasses the whole history of a universe — it is not just some snapshot of how things are, but a whole, possibly matter-filled, spacetime. It describes the state of matter and geometry everywhere and at every moment in that particular universe. Due to its general covariance, Einstein’s theory is not sufficient by itself to determine the time evolution of the metric tensor. It must be combined with a coordinate condition, which is analogous to gauge fixing in other field theories.” [Wp; my bold.]

      In fact, GR seems superficially to be analogous to kin selection as discussed here, to this layman. They are both effective theories (ie they work, but are known to a) ignore substructure b) break down at some parameter choices, say r < c/b). They are both amenable to exact formulations at "weak limits" (energy for GR, selection for kin selection). And it appears they are both believed to work tremendously well, and especially as part of the larger theory (standard cosmology for GR, evolution for kin selection).

      To all appearances, while game theory and the universal wavefunction are of limited use, there are general theories of dynamic systems that capture time implicitly to good effect.

      Got any time for effective theories? If so, good for them and good for you.

      • cooperator
        Posted March 27, 2011 at 4:58 pm | Permalink

        Interesting analogy, but I would argue with the original point that dynamics have to be “imposed” in evolutionary models based on games. For a very simple example, check out the “replicator equation” for game dynamics. I think you will see that it follows from first principles if you accept the notion of birth rates depending on average game payoffs (i.e., “fitness”) and total populations being constant. (One can do much better than the replicator equation.) In any case, the dynamics are not “imposed”. There is nothing like the replicator equation in kin selection theory because it is essentially impossible to write dynamical equations for inclusive fitness. The models therefore try to skip the dynamics and determine an equilibrium directly. Imagine doing this for weather prediction, which is a much easier problem! What a joke.

  12. KP
    Posted March 24, 2011 at 9:52 am | Permalink

    Where is Buggerall State University? Do they have a football team?

    When I review papers, I try to avoid looking at the authors’ names or institutions too much. Avoids the bias that seems to have clearly gotten this paper through the filter.

    Is the peer review process in need of review???

    • NewEnglandBob
      Posted March 24, 2011 at 10:26 am | Permalink

      I got accepted at Buggerall State University but backed out.

      • Dominic
        Posted March 24, 2011 at 10:34 am | Permalink

        I went to Toothickfor University until I was 36, then I went went to a proper one (UCL)…

      • Diane G.
        Posted March 24, 2011 at 11:18 pm | Permalink

        @ NEBob: Groan!
        :)

    • Michael Kingsford Gray
      Posted March 24, 2011 at 5:17 pm | Permalink

      Buggerup University is mentioned in Terry Pratchett’s non-peer-revieved works, (cf “The Last Continent” 1998)

      • Yngve B
        Posted March 24, 2011 at 10:46 pm | Permalink

        Terry Pratchett doesn’t have any peers. He’s in a class all of his own. :-D

        • Michael Kingsford Gray
          Posted March 25, 2011 at 3:39 am | Permalink

          Quite so.
          I find it sad to hear about his rare form of Alzheimer’s that leaves him unable to negotiate rotating doors.
          Even his ailments are in a class of their own.

  13. Dominic
    Posted March 24, 2011 at 10:31 am | Permalink

    No time to read the full debate yet but Nowak & co do not seem to have offered any startling insight that would overturn the huge majority view. Reminds me of arguements about global warming – a tiny minority are given the same space as the vast majority, particularly in the media…

    • Dominic
      Posted March 24, 2011 at 10:33 am | Permalink

      I mean arguments! Not with two ‘e’s – if we had buried my father instead of cremating him, he’d be spinning in his grave!

  14. SteveF
    Posted March 24, 2011 at 10:57 am | Permalink

    I actually think that Alex Wild has the best perspective:

    “I remain unimpressed with the debate. As best as I can tell- this is not my area of research- the fight does not concern anything that actually happens out in the real world. Instead, the bickering boils down to disagreements over which sorts of evolutionary questions are the more interesting ones, and about which body of mathematics is more pleasant to use. These are both matters of subjective opinion. I’ve not seen any demonstration that the competing approaches make different enough predictions to test with empirical data.

    As long as the partisans keep insulting each other in print, though, we’ll see enough bruised egos to prolong the entertainment.”

    http://myrmecos.net/2011/03/23/the-inclusive-fitness-warriors-dig-in/

    • Kevin
      Posted March 24, 2011 at 2:41 pm | Permalink

      Except this IS the controversy in evolution you hear so much about…

      Whether or not evolution is true — no controversy.

      The various mechanisms behind this or that — lots of controversy.

      I know — it’s geeky. Forgive us for not playing creationist whack-a-mole for a couple of posts. We’ll return to our regular programming shortly.

  15. Alex SL
    Posted March 24, 2011 at 2:22 pm | Permalink

    Well, Nature got its controversy but lost its intellectual integrity, becoming something of a scientific National Enquirer.

    Funny, this makes it sound as if that was the consequence of the present affair, and not their modus operandi for the last few decades. Science and Nature generally care for big names, hot topics and controversy more than for good science.

  16. Posted July 28, 2013 at 10:33 am | Permalink

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16 Trackbacks/Pingbacks

  1. [...] http://whyevolutionistrue.wordpress.com/2011/03/24/big-dust-up-about-kin-selection/ 2. [...]

  2. [...] good) mathematics journal. Well today, Jerry Coyne talks about a paper that appeared in Nature: it attacks the idea of “kin selection” in evolution. He makes the following claim: If the Nowak et al. paper is so bad, why was it published? That’s [...]

  3. [...] to John Hawks, I got a link to this post, the last two paragraphs of which is a must read: If the Nowak et al. paper is so bad, why was it [...]

  4. [...] the authors’ re-rebuttal. Jerry Coyne, one of the original critics of the paper on his blog, examines the latest salvos in the argument and what it says about the role of professional reputation in scientific [...]

  5. [...] has posted a few times (here, here, and here) about a paper in Nature by Nowak, Tarnita and Wilson which claims that kin selection is [...]

  6. [...]  Para más información os dejo aquí dos críticas de Carl Zimmer  y Jerry Coyne. Inclusive Fitness: Return to the Wrestling Ring Big dust-up about kin selection [...]

  7. [...] (a professor at the Santa Fe Institute who works on theoretical population biology) has posted on the big kin selection kerfuffle in a piece called “Nowak versus the world.“  Wilkins is apparently with the world: [...]

  8. [...] this paper that have just been published by Nature, some seven(!) months later.  Jerry Coyne has blogged about it, and it’s a good read for reasons not least of which is that he’s an author on one of [...]

  9. [...] http://whyevolutionistrue.wordpress.com/2011/03/24/big-dust-up-about-kin-selection/ [...]

  10. [...] those of you keeping up with the flap on kin selection, there’s a new paper online in the Journal of Evolutionary Biology by F. Rousset and S. [...]

  11. [...] Now this book is not about the paper which attacks the established doctrine of “kin selection”; to read about that go here. [...]

  12. [...] The Big Kerfuffle about Kin Selection (i.e., Nowak et al. verus The World) has finally made the papers: today’s Boston Globe has a piece about it called “Where does good come from?: Harvard’s Edward O. Wilson tries to upend biology again.” I’m not going to reiterate the whole debate, but simply want to give and comment on a few quotes from the paper.  I thought the piece was pretty fair; when I talked to the writer, Leon Neyfakh, he seemed pretty much at sea about what kin selection and group selection really were, but he’s done a creditable job on the article. [...]

  13. [...] Big dust up about kin selection. Biologists E.O. Wilson, Martin Nowak, and Corina Tarnita publish a paper attacking kin selection, the idea that the reproductive success of a gene is influenced not only by its effects on its carrier, but also by its effects on related individuals (kin) carrying the same gene. 130 some odd other biologists respond. Richard Dawkins weighs in. Some talking bears offer a summary. [via] [...]

  14. [...] as selection does act by promoting group behaviors, it does so through inclusive fitness. Only a few miscreants, like Martin Nowak and Ed Wilson, think [...]

  15. [...] intuitive. Ants (and other insects such as bees and termites) are frequently the subjects of hot debate when it comes to kin selection, but their role in evolutionary disputes is over a century old. Charles Darwin discussed them in [...]

  16. [...] in blog form: Jerry Coyne More Jerry Coyne Richard [...]

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