A misguided attack on kin selection

August 30, 2010 • 11:43 am

I don’t know what’s gotten into E. O. Wilson.  He’s certainly the world’s most famous evolutionary biologist, and has gone from strength to strength over the years, winning two Pulitzer Prizes, writing great general books on not only ants but conservation and social behavior.  And he’s kept his hands in the ant work, producing any number of technical papers and monographs. He’s even written a novel!  Frankly, I don’t know how he does it.  I haven’t always agreed with what he says—I think he overreached with the sociobiology stuff, for instance—but you have to admire the guy’s knowledge, breadth, dedication to conservation, and sheer workaholism.

But now Wilson, along with some collaborators like David Sloan Wilson and Martin Nowak, is definitely heading off on the wrong track.  They’re attacking kin selection, maintaining not only that it has nothing to do with the evolution of social insects, but that’s it’s also a bad way to look at evolution in general.   And they’re wrong—dead wrong.

Their latest attack on kin selection is a big paper in the new Nature by Wilson, Martin Nowak and Corina Tarnita, all from Harvard.  They begin by arguing that the classical argument for insect eusociality (cooperatively breeding societies in which “castes” of individuals, like the workers in bees, are sterile and help the queen produce offspring)—an argument based on asymmetrical relatedness—is wrong.  This failure to explain eusociality, they claim, is a severe blow to kin-selection theory.

They’re right about the biology. The “textbook” explanation, based on a higher relatedness of workers to their sisters than to their own potential offspring, no longer seems feasible.  It posits that queens mate only once, but in reality they often mate many times, which destroys the asymmetry of relatedness that supposedly selects for cooperative breeding. Further, other species, like aphids, termites and mole rats, are eusocial but don’t show asymmetrical relatedness.  Finally, lots of haplodiploid species (those in which males come from unfertilized eggs, females from fertilized ones) have asymmetrical relatedness but aren’t eusocial.

But we’ve known all this for years!  Check out the papers by Gardner & West and Strassmann & Queller cited below—they point out the same problems that Nowak et al. present as novel, but as far back as 1998.  There’s nothing new here.

The main problem with the Nowak et al. paper is this: they see the failure of asymmetrical relatedness to explain social insects as a general failure of kin selection to help us explain those groups—or anything at all.  That’s just wrong.  There are alternative explanations for how relatedness explains the evolution of social insects (see the two papers by Strassman and Queller), including the phenomenon of sterile castes.  And, although Nowak et al. claim that “the production of inclusive fitness theory must be considered meagre,” there are many aspects of eusociality that have been profitably investigated, and explained, by inclusive fitness theory.  Here are just a few:  why worker bees commit suicide when they sting; why, when a honeybee colony divides, the remaining queen goes around stinging to death all the other future queens in their cells; why workers prefer to raise rear queens in colonies where their mothers have mated only once, but rear males in colonies where their mothers have mated multiply; and why workers in singly-mated colonies kill male larvae. And there are many others.

Sex ratio theory, in which mothers produce different proportions of males and females, has been a particularly fruitful area for applying inclusive fitness theory.  So has “altruism”—suicidal honeybees are just one example.  And so are parental care and aspects thereof, especially parent-offspring conflict, a field brought to life by Bob Trivers using inclusive fitness theory.  How else can you explain weaning conflict except by a conflict between the mother’s genetic welfare and that of her offspring?

I’m baffled not only by Nowak et al.’s apparent and willful ignorance of the literature, but by statements that are just wrong.  They flatly assert, for instance, that “inclusive fitness theory” is something different from “standard natural selection theory.”  But it’s not: it’s simply a natural extension of population genetics to the situation in which one’s behavior affects related individuals.  I could go on, but a little bird has told me that the big guns in the field will, soon and en masse, answer Nowak et al.’s arguments about both theory and data.

I can’t fathom any motive, either psychological or scientific, for Wilson and Company to repeatedly denigrate the importance of inclusive-fitness theory.  It’s just a shame that, this late in his career, Wilson has chosen to fight the wrong battle. In the meantime, contrast his attacks on the value of kin selection with the summary paragraphs of Strassman and Queller (2007), who, after reviewing the bearing of inclusive-fitness theory on understanding social insects, conclude:

Any scientific theory purporting to account for biological complexity ought to account for this special nature of social insects. Why do their colonies show a degree of apparent purpose lacking in other aggregations, herds, and flocks? The kin selection extension of natural selection theory does explain this; cooperation results from the opportunity to give sufficiently large benefits to kin.

More importantly, kin selection theory has successfully predicted new findings. Although social insect colonies have clocklike design in many respects, kin selection theory predicts who is throwing sand into the clockworks, as well as which gears might be slipped and which springs sprung. Many of the predicted findings, such as sex ratio conflict and policing, were otherwise completely unexpected. The success of this approach shows that the Darwinian paradigm is capable of explaining not just the adaptations of organisms but also how new kinds of organismal entities come into being.

Finally, a big raspberry to the folks at Nature who decided to publish such a strange paper in the interest of stirring up controversy.  If they’d gotten decent reviewers, and followed their advice, it never would have seen print.

UPDATE:  Over at his website, Richard Dawkins has added his own notes on the Nowak et al. paper.  He doesn’t like it either, and for many of the same reasons.


Nowak, M. A., C. E. Tarnita and E. O. Wilson.  2010.  The evolution of eusociality.  Nature 466: 1057-1062.

Queller, D. C., and J. E. Strassmann. 1998. Kin selection and social insects. Bioscience 48:165-175.

Strassmann, J. E., and D. C. Queller. 2007. Insect societies as divided organisms: The complexities of purpose and cross-purpose. Proc. Nat. Acad. Sci. USA 104:8619-8626.

West, S. A. and A. Gardner.  2010.  Altruism, spite, and greenbeards.  Science 327:1341-1344.

80 thoughts on “A misguided attack on kin selection

  1. I don’t suppose you could recommend any lay-friendly reading material about the current thinking regarding the evolution of eusociality?

    I had just wrapped my head around the asymmetrical relatedness idea — and then only partially — and now you say it is wrong! Dangit…

    1. I don’t know of any offhand but I’ll check. In the meantime, for others, I’ll reprise the (probably incorrect) asymmetry argument:

      In haplodiploid species, whose males come from unfertilized eggs and females from fertilized ones, a given female shares three-quarters of her genes with her sisters (if her mother mated only once). That’s because all offspring get an identical half of their genome from their father (who has only one set of chromosomes and passes it on intact to his kids), and the remaining half of their genome is 50% shared with their sisters because of recombination in the mothers. In other words, the proportion of shared genes between a female and her sisters is 50% + 1/2(50%) = 75%, or 3/4 of the genome.

      But a female shares only HALF of her genes with her own offspring. Therefore, you could argue—as early workers did—that any gene that “tells” a female to become sterile and produce more sisters (as workers do in honeybee nests) would leave more copies than a gene that “tells” her to have her own offspring. This asymmetry was the early explanation of why eusocial insects have sterile worker females.

      The problem is that if females mate more than once, then their female offspring are not more highly related to their sisters than their own offspring, eliminating the evolutionary impetus for sterility. Also, although females are related by 75% to their sisters, they’re related by only 25% to their brothers. Since they’re related by 50% to their own sons, it would pay them, as far as males are concerned, to have their own offspring rather than help the queen produce more sons. Considering both male and female offspring, then, there seems to be no net genetic asymmetry that would select for sterility. But, as I said above, there are other ways that relatedness, even if symmetrical, could promote the evolution of eusociality.

      For this and other reasons, the “haplodiploid” argument for the evolution of cooperative breeding is no longer very convincing.

      1. And if I remember correctly, empirical studies show that species/colonies with multiply mated queens tend to have more intra-nest conflicts wherein un-mated females lay unfertilized (i.e. haploid, i.e. males) than species/colonies with singly mated queens, though I could be misremembering. Is this not a verified prediction of inclusive fitness?

        Caveat emptor. I’m a tad hazy as it has been nearly 10 years since I read this literature regularly.

    2. There’s nothing wrong with the theory of the haplodiploid asymmetry.You definitely haven’t wasted your time wrapping your head around it. You’ve wrapped your head around a correct piece of theory. It’s just that, in practice, many social insect queens mate more than once, thereby neutralising the asymmetry. Hamilton was well aware of this practical difficulty, which was one reason why haplodiploidy did not bulk large in his exposition of inclusive fitness theory.

      Richard Dawkins

    3. not really lay reading, but I always recommend the collected works of WD Hamilton:

      Narrow Roads of Gene Land.

      Moreover, for a more recent review of the evolution of social behavior in general, there was a volume published in Evolutionary Biology a few years back that IIRC is open access:


      as a general comment, those thinking the paper under discussion here is something “new” must be new to the writings of DS Wilson.

      there is nothing new in this paper, and all of it has been roundly and correctly critiqued before.

  2. I predict another spate of “Darwin was wrong” news reports.

    Seems like a review article (I don’t have a subscription and don’t want to pay $32). Do they have any new data to support their hypotheses?

    1. No new data, nor any new arguments, either. Wilson and his colleagues have been making these same arguments for several years, and they’ve already been answered by other workers in the field. But, like creationists, these guys go on making the same fallacious claims.

      1. Then I’ll definitely wait for the counter-argument before I spend $32 or make the less-expensive trip to the library that has the subscription.

        Should I butter the popcorn?

      2. Interesting, as I’m reading the replies of the 139 et al, months later.

        “Creationists”? Even with allowance for hyperbole, you’ve got to be kidding. I thought Sloan’s response to the 139 was very good.

  3. “Although social insect colonies have clocklike design in many respects, kin selection theory predicts who is throwing sand into the clockworks”

    That could also be said of individual organisms and non-cooperators like cancer cells, or of genomes and non-cooperators like parasitic DNA. Or even symbionts that are sometimes mutual and sometimes parasitic. At any level of biological organization there are circumstances in which cooperation prevails and in which non-cooperation will occur.

    So maybe group selection (using ‘group’ as a term for any assembly of cooperating units, whether a genome, organism, symbiont, or colony) AKA individual fitness (‘group’ regarded as an individual) is a special case – when cooperation prevails – of the kin selection of those constituent units.

  4. Bit of a tangent but if interested in a bit of scifi that touches on the subject of eusociality, then grab a copy of Frank Herberts’s book “Hellstrom’s Hive”. It’s great.

  5. I’m reminded of the controversy on the pages of New Scientist a few years ago (I think it was 3 Nov 2007) in which E.O Wilson and David Sloan Wilson seemed to champion group selection as a major driving force in evolution.

    Prof. Dawkins wrote a letter to NS criticising this idea, I think correctly, but it was rebuffed by E.O. Wilson himself.

    As a layperson, the article seemed to me an attempt to resurrect “group selection” as a viable theory after it has its ass kicked in The Selfish Gene three decades earlier. As far as I know, no-one has managed to demonstrate any mechanism by which group selection could work without it being undercut by “selfish” agents (genes) acting at a more basic level.

  6. I’d recommend that young biologists follow this closely. It’s going to provide you with something to teach your students about the sociology of the scientific community. I will confess that it is not yet clear to me what that something will be.

    In present company, I will assume that I am insufficiently informed to recognize the flaws in Nowak et al. that are so apparent to others.

  7. You’re mostly correct, but, as always, it’s a bit more complex than that. The current consensus is that group selection (indeed, selection at all levels) does occur. In fact, it’s a unavoidable statistical fate. However, selection at the individual (or genetic) level is usually stronger and usually opposed to selection at other levels.
    It’s been a while since I’ve looked at that stuff, but I think that Leticia Aviles at UBC did some work with colonial spiders that operated that exhibited those special conditions.

    1. Well yes and no. Group selection is “valid” in the same sense that individual selection is “valid” — both are only valid insofar as what is really happening is differential success of genes reproducing.

  8. Did E.O. write it himself or is his name just on there? Is it senescence creeping in? I’m always surprised to see he’s still about and doing things. It needn’t have anything to do with age though; I just remembered that a lot of very good scientists from the past have all had their share of just plain wrong ideas. Even Einstein, after decades of thinking about it, gave up on his Grand Unified Theory (or was it the “Theory of Everything”) and had even told people it’s not going to work (of course many of those people didn’t believe him and just went on).

        1. No, he’s undoubtedly brilliant. Also, he has a very helpful webpage with large numbers of his papers available to read:


          Well worth checking out

          On a general note, it’s positive how many evolutionary biologists put their papers online for anyone to read. Michael Lynch and Gunter Wagner are other good examples.

  9. Well, to be honest, I have never felt that the kin selection explanation of eusociality is very convincing. When I first read of it as a student, my immediate reaction was: “but what about termites”?

    This is not saying that inclusive fitness does not tell us anything relevant about parent-offspring conflicts, but it fails as an explanation of eusociality the second you realize that there are eusocial organisms that have diploid males, and that is shrewdly ignored in many books or articles discussing eusocial hymenoptera. In that sense, I welcome more awareness-raising discussion, even if it should get started by a questionable argument.

    1. The fact that termites are eusocial simply demonstrates that relatedness asymmetries (like you get with haplodiploidy)are not necessary for the evolution of eusociality. However, termite eusociality in no way undermines kin selection as an explanation for eusociality. After all, termite colonies are composed of family groups (i.e. kin selection is a viable explanation) as is the case for all other eusocial species. There is a tendency to confuse the “haplodiploidy hypothesis” with kin selection in general. Also, it should be noted that a fairly recent paper using ancestral reconstruction showed that monogamy is most likely ancestral in eusocial lineages, which detracts somewhat from the argument that multiple mating by queens argues against the haplodiploidy hypothesis. Plus, eusocial thrips are haplodiploid, suggesting that there *might* still be something to the haplodiploidy hypothesis. Of course ecological factors, which determine the costs and benefits, are also very important in all cases. Relatedness only alters how large the B/C ratio has to be.

    2. What books have you been reading that have made the claim that eusociality requires haplodiploidy? That may be your first problem. Eusociality is predicted under conditions that do not require haplodiploidy, though as others point out, under certain areas of parameter space, you can get eusociality under haplodiploidy much easier than for diploidy. It just so happens that the parameters that promote such conditions may not be common (i.e. queens are often multiply mated) and so the hymenoptera-centric explanation may not be very useful. But that doesn’t say very much about inclusive fitness in general or its influence on the evolution of eusociality in particular.

    3. Normal diploid offspring are as related to each other (siblings) as to their parents. So devoting resources to creating more siblings is just as viable a strategy as producing offspring.

    4. I have no problem with kin selection and messed up my first comment.

      The thing is just I have read several popular science explanations giving the haplodiploid explanation, and I never understand why we need convoluted ideas like entirely instinct-driven workers “deciding” to raise their siblings instead of children when a very simple one is available: those queens that can produce infertile slaves to help them are able to out-compete those that cannot. If you are a honeybee worker that “decides” to raise her own family, you’re toast and your mother is toast. End of story.

      1. If the workers were clones of the queen your queen-making-slaves idea would work — for the same reason the all the cells in your body could be seen as “slaves” working ultimately for the benefit of your the germ-line cells in your gonads, which are the only cells that get a chance to pass on copies their genes via sperm or egg to the next generation (mutations in your germline can be passed to offspring, for example, but mutations in your heart, skin, or brain cell a passed only to their daughter cells and ultimately will die with you).

        The workers get half their genes that come from the father, and it is not necessarily in the interest of those genes (from the father) to help the queen to produce daughter-queens unless the father’s genes are also in those daughter-queens (which may not be the case sincwe queen mates with multiple males). It could potentially be in best interest of genes-from-father for the worker to reproduce directly. And since the workers do not get all the Queen’s genes, the Queen’s daughter-queens may not share all the worker’s genes-from-mother either. So it is a question of kin-selection cost benefit whether the genes-in-worker a best served by the worker staying sterile or reproducing on its own.

        The idea of queen *forcing* workers to be slaves somehow is debunked because the weaknesses that allow the workers to be thus force would not be selected, unless the same gene (and hence same weakness) was in the queen. After all, before there were queens, how was it decided who reproduced? There must have been transition stages of colonies with multiple queens, dominance competitions, and so forth. In fact you will find types of wasps (and I think ants) that exhibit a spectrum from “all (or nearly all) reproducers” to “one and only one queen-mother”.

        1. I understand the idea, but my point is: what if the decision is between having genes for a worker caste and not being competitive enough to survive? The latter situation would not help the genes in an egg-laying daughter very much, no matter what their interest.

          Also, I simply don’t buy the weakness also in the mother argument. That is what specialization is; the “weakness” of my somatic cells not to be able to reproduce is also not shared by my parent’s gametes. And note that that also goes for chimeras.

          1. Alex, this forum is not a good place for a more extensive answer. What you say about the queens is *approximately* true given certain assumptions about the current state of the species in question (i.e. that the queen/caste system is pretty much already established). But it is not a complete picture. Basically (forgive me) you are thinking about the question too simplistically — it is not a question a sudden mutation that pops up and causes the worker bee who has it to instantly run out an “start a family”, evolutionary changes to worker behavior would be much more gradual. Even if it was as simple as you describe, the conclusion that both worker and colony “would be toast” is just an assumption.

  10. It’s not too surprising that David Sloan Wilson is also among those challenging kin selection. I mean, what else do you expect from a guy who denied his son his birthright machete?

    Anyway, I wonder how long will it be before the creationists start spinning this as “proof” of a crisis in evolutionary theory. I give it less than a week…

  11. What do you mean “the big guns”? Don’t be so modest. You are one of the big guns… aren’t you?

    I’ve been waiting for some big guns to come out against this foolishness… your blog is the first I’ve seen.

    I never much bought the haploid nature of bees & ants and *necessary* for eusociality (and obviously it isn’t given termites, etc.). After all, ordinary diploid offspring are as closely related to their siblings as to their parents, so it is just as advantageous to help an diploid parent reproduce as to reproduce oneself. Or is there something I’m missing in that line of reasoning?

    I think Nature can be forgiven, considering E.O.Wilson’s stature in the field. If I were an editor, my thinking would be to let the larger community of evolutionary biologists as a whole hash it out. Reviewers are just a first line of defense. The critique after the publication, which is happening now, is where the real battles are fought.

    Wison is very fond of his ants and clearly *wants* very much to see more than the selfish gene at work in the evolution of social behaviors.

  12. The more biology I read, the more pervasive I find a particularly bad notion – that an explanation must be singular, must apply always, and must have equal applicability between the present and the past.

    In the minds of some, it seems, complex webs of causation are just too much to think about. If a contributing factor cannot be said to act alone, or have its effects isolated by experiment or model, then it cannot be a factor at all. It’s really abysmal reasoning, and it’s shocking to see it practiced by people who should know better.

    Of *course* the fact that females are more related to sisters than their own offspring has influenced both the origin and development of eusociality in haplodiploid insects. That doesn’t mean it’s either necessary or sufficient – termites and solitary haplodiploids show that well enough.

    An analogy of what sloppy thinking I see here on the part of Wilson and his new compadres. Say you have a certain type of car which crashes more frequently than others of its type. Someone notices that the wheels seem to have a design flaw which causes the tires to blow out very often, and calls this a contributing factor in the increased accidents. Perfectly reasonable. Now someone comes along and plays up the accidents where the tires were intact, and says, “See!? These accidents cannot possibly be caused by a faulty wheel design.”

    More directly to the case of multiple matings with haplodiploids, I have to say I disagree with Jerry’s characterization of its affect on sister-sister relatedness. Sisters with a common father have 3/4 relatedness, while those with different fathers 1/2, just as their own offspring would have. But it’s not about individual relatedness. It’s about the odds of a gene impacting a copy of itself in another body. No matter how many times the queen mates, a gene in a haplodipoid female will always have a >50% chance of finding itself in a sister, averaged over the hive (ignoring queen replacement effects in this case). It will always be exactly 50% for offspring. Even if you assume it’s a contest between 51% and 50%, consider what I’ve read many times now about mice and elephants – assuming a mere 1% increase in size, it’d take only about 1000 generations to turn a mouse into an elephant. Even such tiny differences, over millions of years in a rapidly reproducing insect, will have an immense impact.

      1. I didn’t forget about the males, but didn’t address them because I was well on my way to a novella already.

        Haplodiploid males are a wash in this scenario, as it doesn’t matter how many times the queen mates – workers will be equally related to each male they rear (again, adjusted for queen replacements), there being no paternity.

    1. Assuming these differences and everything else equal, wouldn’t a larger hive see smaller differences fixate? In your example, easier for mice to elephants than the reverse under selection.

      [Ergh! A math model would be easier to pick apart and see the clockwork in.]

  13. you have to admire the guy’s knowledge, breadth, dedication to conservation, and sheer workaholism.

    And also his writing–some of it’s really beautiful.

  14. These were precisely the same kinds of objections that were raised in my mind by this paper.

    It certainly didn’t help that when I heard advance word about the paper on the journal’s podcast that the journalists discussing the paper couldn’t come up with a clear synopsis.

  15. It’s always sad when great people screw up their legacy with bullshit as they get older. Like Napoleon invading Russia and Einstein with quantum theory.

    1. Einstein facilitated quantum and atom theory both, despite his misgivings. If you want someone who really screwed up the small world, it was Planck that wouldn’t accept the implications of his discoveries at all.

      No, Einstein’s screw up was that he took the success of GR, an effective theory, as a valid research strategy for a fundamental theory _and_ that he isolated himself from the science. Either one in isolation would have been immensely much more productive for science – together they were a sure “kill”.

      I’m not a biologist, but in this case I have to hark to Thanny’s description. I find the adaptionist/drifters (?) battles funny, because for me they are about equally valid research strategies (you can/have to test one mechanism first – even the less likely one, if you want to be less successful), but in principle they can communicate and adapt. (Or drift, whatever makes their personal world go around. :-D)

      That doesn’t seem to be the problem here.

  16. Quoting from Carl Zimmer’s article on nytimes online, “Dr. Ratnieks argues that the Harvard researchers cannot rule out kinship as a driving force in social evolution because their model is flawed. It does not include how closely related animals are”. That seems to me a serious flaw.

    As my first comment in this blog I would like to congratulate Jerry for his homonimous book. It is just great 🙂

  17. To expand on the point about haplodiploidy being incidental to Hamilton’s classic double paper of 1964, out of 49 pages (in the *Narrow Roads of Gene Land* reprint), the haplodiploidy hypothesis occupied a mere three and a half pages. This was followed by another three pages discussing the fact that Hymenopteran queens often have multiple mates — precisely the point advanced by Nowak et al as a ‘new’ criticism! Hamilton then went on to discuss the case of the termites (which are not haplodiploid) thereby anticipating another of the ‘new’ criticisms. The termites, as Hamilton also pointed out, have a completely different tell-tale predisposition to eusociality under his theory, namely recurrent inbreeding, which raises the coefficient of relatedness in a way parallel to the ‘haplodiploidy effect’.

    Given that Nowak et al seem to think haplodiploidy is central to Hamilton’s theory, I am astounded that they totally fail to mention the work of Robert Trivers and Hope Hare on sex ratio biases in Hymenoptera (see *The Selfish Gene* for a full discussion of this work, which is alluded by by Jerry above). Trivers and Hare calculated optimal sex ratios from the point of view of a queen, and from the point of view of a worker ant, given haplodiploidy. If the queen exerts power over the ratio of males to females, the stable ratio of colony investment in males versus reproductive females would be 1:1. If the workers have control over the sex ratio, there would be three times as much investment in females as in males. They went on to measure the actual ratios in 20 species of ants and found a female bias as per the haplodiploidy prediction. There was even an ‘exception that proves the rule’ in the form of slave-making species whose workers have no power because the work is all done by slaves. The Trivers/Hare study has been criticised on various grounds, but it is astonishing that Nowak et al ignore it completely.

    In any case, the most important point is that Hamilton’s theory does not — and never did — stand or fall by the enigmatic special case of haplodiploidy. On the contrary, by far the bulk of work using the theory has been done on ordinary diploid organisms, and the bulk of Hamilton’s own thinking on the subject concerned diploid organisms. Hamilton’s theory of Inclusive Fitness is not something set apart from ‘Standard Natural Selection Theory’. It *is* Standard Natural Selection theory, made complete by filling in a logical implication that had previously been overlooked.

    1. Who could ask for anything better than the clear explanations of Jerry Coyne and Richard Dawkins! May I suggest a collaborative book?

    2. “Hamilton’s theory of Inclusive Fitness is not something set apart from ‘Standard Natural Selection Theory’. It *is* Standard Natural Selection theory”
      I think the same misunderstanding is often made with Sexual Selection as well, which to me is obviously a subset of natural selection! (And if I remember well Jerry Coyne states it clearly in his WEIT)

  18. From what I have seen, Boomsma’s Monogamy hypothesis explaining eusociality has gained some steam. It was mentioned by name in the West et al. (2010) paper cited above and those authors seem quite content with Boomsma’s explanation. Specifically, Boomsma took the standard “rB > C” argument, modified C so that it was “0.5B > 0.5C” (because offspring on average are related to the parent by 0.5), and then cancelled to get “B > C” so that any factor tipping the balance towards helping siblings will start to push a system towards cooperative breeding and possibly eusocial castes. I wonder if Nowak et al (I haven’t read the paper or the 41 pages of supplementary material yet) addressed this idea.

    1. To take this one step further, in many ways, the B>C is the important part of Hamilton’s equation. The fact is that even if you are extremely highly related, as might be found in an inbred and haplodipoid population you the total of the inequality still must outstrip the costs. What often seems to happen is that people become stuck on the relatedness component at the expense of the b and c. In part, that is probably because b and c are far more difficult to actually evaluate. That is because initially it seems as something that can be measured simply as number of offspring, but in fact these number represent the sum total of all the other ecological factors.

      The second issue is that these arguments tend to be very ant/honey bee centric. When one starts looking at primitively social organisms such as sweat bees and many wasps, we find that things tend to become messier in many of the ways that we would predict. This includes workers that are not entirely sterile and lay eggs, colonies that consist of unrelated workers but which gain indirect fitness in other manners, queens that bully their workers etc.

      Finally, I would add the subtle reminder that really there should be an r term on both sides of the inequality. So, really it might be best to consider the inequality as rB>rC.

  19. “Finally, a big raspberry to the folks at Nature who decided to publish such a strange paper in the interest of stirring up controversy. If they’d gotten decent reviewers, and followed their advice, it never would have seen print”. Right, just as in Marc Hausers’ case.

    1. Here’s a similarity to the Hauser case:

      Hauser got a lot of attention and prestige because his work was believed to be relevant to a deeper understanding of the origins of the human mind and morality – and surely that had profound implications well beyond the academy. Moral philosophy, criminal law, maybe even education and so on.

      For decades, many believed that since inclusive fitness had something to tell us about how our social behaviors came to be it must be relevant to multiple fields of human endeavor, perhaps (even with the perfunctory handwaving about the naturalistic fallacy) informing us on how best to conduct these.

      But no, there’s nothing riding – outsides of a few corners of academia – on whether Nowak/Wilson/DS Wilson are right or Dawkins et al are right. And these are just rival schools of adaptationist selectionism a few shades apart. It doesn’t even matter whether selectionists or Lamarckians or even theistic evolutionists are right, and whether the subject of the debate is ant evolution or hominid evolution. Because only proximate mechanisms are of practical, that is non-academic, importance when it comes to behavior.

  20. I’m much more interested in hearing an analysis of the mathematical results of the paper.

    Are they new? Are they wrong? Are they irrelevant?

    At the end of the day, natural selection should be decoupled from biology and grounded in fundamental mathematical rules. I get frustrated reading some discussions of natural selection because it seems like a conversation between armchair natural philosophers. Surely if natural selection can be described mathematically, everything else is secondary.

    1. “At the end of the day, natural selection should be decoupled from biology and grounded in fundamental mathematical rules”.
      Uhm, that sounds like putting the cart before the horses, as the saying goes (I think; in Italian they’re oxes). Of course scientific data should be mathematically describable, but one should not follow mathematics so much as to forget the real organisms – at least as long as we’re dealing with maths applied to biology and not pure maths. And good mathematics does not necessarily mean good biology. For instance, as I have already pointed out (well of course it wasn’t really me, I just quoted an article from Carl Zimmer), Wilson and Nowak’s model does not include how closely related animals are. This could undermine the validity of their study even if the mathematics per se is flawless

      1. I can only comment on the 43 page PDF “supplementary material” (I don’t have access to Nature.com) but it appears to be a more fully worked out disquisition on the subject than whatever the article itself contains.

        From my reading, Nowak, et al., do not include relatedness in their model, because they have found that it isn’t required in the end. They do work through their model to include relatedness but demonstrate (to their satisfaction anyway) that it ultimately doesn’t factor into the results so it is ultimately irrelevant.

        I would like to see this aspect of the paper addressed by its critics. Why is this model wrong?

  21. Appalling. I wonder why Prof Dawkins wasn’t asked to review the paper. Any guesses on who did (review it)?

    It all has the foul smell of another MacMillan Publishing Co. publicity stunt, like “the memory of water”…

  22. It looks like many here have missed what the terms of this controversy are, simply because they are in diapers philosophically.

    Wilson’s & coterie’s change of mind was forced by 1999 work by James Hunt who studied multiple origins of sociality in a wasp phylogeny in which all the species had about the same “kin selection potential” and yet he found that sociality evolved only when there were very strong “ecological” incentives (Hunt, J. H. 1999. Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution 53: 225-237).

    But since ~2005 EO Wilson, Hoelldobler, etc, have hijacked the controversy.

    Some people have indeed started realizing that crucial for the existence/persistence –and thus for the evolution– of animal societies is not (or not so much) “kin selection” but rather the fact that there are very rewarding ecological niches out there in which biomachines that adopt group-approaches to foraging and interference competition are much more effective trophically than are biomachines which adopt “solitary-consumer/fighter/reproducer” strategies.

    This means that the evolutionary-genetical success of the genetic programs encoding such group behaviors is fully subordinate to the existence of such ecological opportunities!

    In other words: people have begun realizing that, e.g., “altruism” is also a wining ecological strategy, rather than just an example of the promotion, or not, of altruism genes and the rejection of cheater genes.

    The social-ant colony, e.g., is an ecological machine that out-competes at the foraging- and interference-competition level most other organisms in almost any terrestrial ecological setting, i.e., a social-ant colony in the field cannot be reduced natural-historically and evolutionary-historically to just an example of an ESS immune to “selfishness” mutations that may undermine the genetic encoding of its sociality.

    EO Wilson indeed has always made a big deal of the fact that ant species monopolize nearly 70% of the insect biomass on earth, but he did not realize the implications of this until the wasp guy rubbed it to him and his coterie while they were still happily repeating the empty syllogisms of kin-selection numerologists [who meanwhile have even almost managed to deny Darwin (sic!) the credit for explaining the existence of sterile ants, etc., by appealing to sacrifice that benefits the reproduction of relatives, i.e., kin selection, duh! see “on the origin…”]

    This 70% means that evolution by “natural selection of individuals” delivers niche-occupancy strategies that suffice to claim only ~30 of the trophic energy monopolized by the insect Bauplan (assuming termites and other social insects are insignificant biomass-wise).

    The situation among many mammals is the same. Wild-dog packs, e.g., beat the hell out of tigers, and biomass wise the packs must dominate…

    It is time for gratuitous faux-a-prioristic misused-math arguments to be confronted with ultimate natural-historical facts.

    And it is also time that the too-many cheapo-applied-math peddlers posturing as evolutionary biologists learn that “natural selection” is not the same as “evolution by natural selection”, that differential fitness is always caused by differential ecological performance (and never by “genes”), and that evolution by natural selection is just something that “may” happen to genes provided that there is differential ecological performance at some level of biological organization, which however does not “prove” that the differential ecological performance is at the level of genes.

    In other words, Sober’s 1984 [1984 sic!] book “The Nature of Selection” should be required reading for every evolutionary biologist.

    PS. I found this very recent paper below that studied this ecological group-performance vs. “kin-selection” issue within a clade of sponge-living shrimp.


    Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

    Author(s): Duffy JE (Duffy, J. Emmett)1, Macdonald KS (Macdonald, Kenneth S.)2

    Source: PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES Volume: 277 Issue: 1681 Pages: 575-584 Published: FEB 22 2010

    Times Cited: 2 References: 62 Citation MapCitation Map

    Abstract: Eusocial societies present a Darwinian paradox, yet they have evolved independently in insects, mole-rats, and symbiotic shrimp. Historically, eusociality has been thought to arise as a response to ecological challenges, mediated by kin selection, but the role of kin selection has recently been questioned. Here we use phylogenetically independent contrasts to test the association of eusociality with ecological performance and genetic structure (via life history) among 20 species of sponge-dwelling shrimp (Synalpheus) in Belize. Consistent with hypotheses that cooperative groups enjoy an advantage in challenging habitats, we show that eusocial species are more abundant, occupy more sponges, and have broader host ranges than non-social sister species; and that these patterns are robust to correction for the generally smaller body sizes of eusocial species. In contrast, body size explains less or no variation after accounting for sociality. Despite strong ecological pressures on most sponge-dwellers, however, eusociality arose only in species with non-dispersing larvae, which form family groups subject to kin selection. Thus, superior ability to hold valuable resources may favour eusociality in shrimp but close genetic relatedness is nevertheless key to its origin, as in other eusocial animals.

  23. Jerry,

    I have followed this selfish-gene vs. group selection debate for years, and in blog comments and forums have always defended the selfish-gene position. However, since the 2010 Nowak et al Nature paper, something has nagged at me — that buried in their opaque mathematics in the appendix of that paper and their poor choice to frame their ideas in terms of “group selection”, they have a valid point. It may be a point well known and understood to biologists, so the debate is about interpretation and terminology… or it may be a somewhat novel point (although from a mathematical perspective it should be almost as obvious as Hamilton’s rule).

    Here is what I *think* he might be getting at: suppose you have a trait with reduces the reproductive success of a individual *relative* to the “group”, but which enhances the overall reproductive success of the group as a whole more than enough to offset the personal “sacrifice”. The “group” need not be related in any way and might be defined merely by proximity (local neighborhood). Such a trait would certainly be favored by natural selection, simply by considering the net effect (to increase reproductive success of the carrier).

    To clarify with a concrete example: suppose I have a behavioral trait which gives my immediate neighbors, or my “group” a 0.1% reproductive advantage over me, but also gives my group (including me) a 0.2% advantage over neighboring groups. I still get a 0.1% net advantage as compared to the global population. My progeny who carry the trait become less frequent among the local population but more frequent globally. This trend will continue towards some evolutionarily stable distribution with the global population.

    Just to further show how this kind of trait can lead to apparently altruistic behavior, consider that the .1% or .2% advantages are statical averages. And further suppose that the .1% “sacrifice” is virtually guaranteed with only a little variation, but suppose that the .2% payoff for the “group” is the result of a 100% payoff which only happens .002% of the time. Such a behavior would easily be seen as “self sacrificing” as the connection to the payoff would not be obvious.

    A trait like this is encompassed by selfish-gene theory which ultimately only cares about the net effect. But such a trait would result in behaviors which appear altruistic with respect to the local “group”. A trait like this would actually be a special case of “win-win” cooperative behavior — might call it “win-WIN” cooperation to emphasize the lop-sidedness of who benefits.

    If this is the what Nowak, Wilson, et al, are trying to get at, they are not doing a particularly good job of explaining their position. It certainly does not support “group selection” in the sense of groups as units of selection. (It does not have much if anything to do with Wilson social/political view either as far as I can tell)

    However, in discussions of the evolution of altruism (or seeming altruism) I have read (such as here, in Dawkins’ books, other blogs, forums, etc.), this kind of asymmetric, indirect “win-WIN” effect never seems to come up.

    1. Just occurred to me, maybe I should call it “lose-WIN” to emphasize not just the lopsidedness, but also to emphasize the initial sacrifice which results in a more-than-offsetting payoff.

  24. Just finished the Wilson book. He claims that there is mathematical proof of his position. Can anyone point me to where I can find such a proof, and also to any mathematical critique of it.


  25. A trait like this is encompassed by selfish-gene theory which ultimately only cares about the net effect. But such a trait would result in behaviors which appear altruistic with respect to the local “group”. A trait like this would actually be a special case of “win-win” cooperative behavior — might call it “win-WIN” cooperation to emphasize the lop-sidedness of who benefits.

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