The kin selection argument continues, with those denying its importance holding firm. They’re wrong.

In 2010, Martin Nowak, Corina Tarnita, and E. O. Wilson wrote a paper in Nature (reference and link below) arguing that “kin selection,” selection based on relatedness (shared alleles among nestmates) was not—as had long been maintained—a key factor in the evolution of “eusocial” insects. (Those are species in which there are nonreproductive “castes” of workers, with some tending the brood) while reproduction is limited to one or a few “queens”.)

The problem with this paper was their dismissal of relatedness as an important factor in the evolution of this remarkable social system (eusociality isn’t just limited to insects; we also see it in some crustaceans and in naked mole rats). Nowak et al.’s “model,” such as it was, did not allow the degree of relatedness to vary, so there was simply no basis for their claim that relatedness was not “causal” in the evolution of eusociality. In fact, there was already evidence that kin selection was important in the evolution of eusociality. As I wrote in March of this year:

But the evidence for kin selection and relatedness is still clear. For example, eusociality in Hymenoptera has evolved several times, but always occurred in an ancestral lineage in which queens mated singly rather than multiply: a statistically significant finding (Hughes 2008; reference and free link below). That’s important because in such cases offspring are more related to each other than are offspring produced by different fathers. Further, Bob Trivers showed that other patterns in bees, ants, and wasps—especially the observed ratios of males to reproductive females in colonies—also followed the dictates of what kin selection predicted. There are still other behavioral recognition experiments of kin versus non-kin supporting the importance of relatedness.

The 2010 paper by Nowak et al. was criticized on these and other grounds by virtually every evolutionary biologist working on the evolution of social behavior. One critique had over 130 authors! But Nowak et al. have stood their ground, largely alone in their views with the exception of David Sloan Wilson, who, for reasons I can’t fathom, argues that Nowak et al.’s “group selection” argument is right, and has just published a note on his website called “Mopping up final opposition to group selection.”  As the battle winds down, D. S. Wilson has declared victory for the wrong side!

I’ve continued to monitor the controversy, and you can find the links to my many posts here. The latest critique of Nowak et al. was leveled by Liao, Rong, and Queller (link and reference below), which I reported on here.  I won’t go into their findings in detail, but Liao et al. did what Nowak et al. should have: they made models in which relatedness was allowed to vary, for that’s the only way to see how important kin selection (i.e., selection based on relatedness) is in the evolution of eusociality. As I wrote in that post:

Unlike Nowak et al., Liao et al. varied total relatedness by allowing a certain fraction of offspring in the nest to be unrelated to the “queen” rather than simply her clones. (This could occur by immigration of insects from other nests, or by queens laying eggs in other queens’ nests.) What they found is that relatedness indeed makes a big difference: under conditions in which worker behavior is affected by their own genes rather than just the queen’s, eusociality evolves much more easily when relatedness between queen and “worker” is higher. In other words, higher relatedness (kin selection) is causal in this circumstance, not just a consequence of the evolution of eusociality. Nowak et al. were wrong, and all the statements of this group about the uselessness of kin selection based on this model are also wrong.

Nevertheless, Nowak and his colleagues are showing a characteristic trait of some scientists: a complete refusal to admit that their critics had any valid points at all. In response to the Queller et al. paper, Nowak and Benjamin Allen just published a note in PLoS Biology (reference and link below) defending the original result and dismissing Liao et al.’s criticisms.  Responding to that in a one-page note in the same issue, Queller, Rong, and Liao once again show how Nowak et al. (2010) were misguided and misleading, and that the subsequent Nowak and Allen paper apparently concedes ground while pretending not to do so.

Here is what Nowak and Allen now contend (I’m summarizing what I see as the two important points):

1. Nowak et al. never said that relatedness was unimportant. From their paper (“LRQ” is Liao, Rong, and Queller’s paper modeling variation in relatedness; “NTW” is Nowak, Tarnita, and Wilson’s original paper):

Why do LRQ investigate such models? They present NTW as saying relatedness does not matter in general, but this is incorrect. Instead NTW write, “Relatedness does not drive the evolution of eusociality. We can use our model to study the fate of eusocial alleles that arise in thousands of different presocial species with haplodiploid genetics and progressive provisioning. In some of those species eusociality might evolve, while in others it does not. Whether or not eusociality evolves depends on the demographic parameters of the queen (…), but not on relatedness. The relatedness parameters would be the same for all species under consideration”

Nowak and Allen also note (see their Figure 1), that among the many species that have the kind of mother/offspring association that could promote eusociality (“progressive provisioning,” in which offspring are continuously fed in nests), only a few have evolved eusociality.

I see this as disingenuous. NTW did indeed argue that relatedness is unimportant in the evolution of eusociality, precisely the problem that LRQ investigated, showing that relatedness was important. As for the fact that eusociality didn’t evolve in a lot of progressive-provisioning species, everyone, including Queller and his colleagues (and me!) admits that factors other than relatedness can influence the evolution of eusociality. After all, there are ecological factors that affect the benefits and the costs of evolving sterile castes, fertile queens, and the like. But the results of Hughes et al. and of Trivers suggest strongly that kin selection was important in the evolution of eusociality. Neither NTW nor Nowak and Allen mention these results. Leaving out discussion of results that support your opponents’ position is not a good way to behave in science.

2. Nowak and Allen argue that Liao et al.’s models of varying relatedness are biologically unrealistic. You can read their criticisms themselves, and I’m unable to judge, not knowing much about the biology of the Hymenoptera, whether these particular models correspond to situations that actually obtain in nature.

I asked my friend Phil Ward, a professor of entomology at the University of California who works on Hymenoptera, about this issue, and he replied that while Liao’s “mixing model” seems a bit contrived, “there is probably enough nest usurpation and nest-sharing among non-social bees and wasps to generate significant variation in relatedness among interacting groups of individuals, if not exactly in the manner modeled by Liao et al. (2015).”

I agree. Surely the degree of relatedness can vary among nests in nature, however that happens, and if relatedness is “causal,” (which Nowak et al. deny but Liao et al. affirm), then that will affect the likelihood of evolving eusociality. To dissect the specific models without addressing whether something might alter relatedness in non-social hymenopteran nests is to throw out the baby with the bathwater.

That said, we clearly need more empirical work on the biology of non-social Hymenoptera that build nests so that we can answer the question that Nowak and Allen (and many others) have posed: Why have most of these species not evolved eusociality? The answer likely involves some combination of ecology, behavior, and relatedness.

In their very short response to Nowak and Allen, Queller et al. can be quoted directly, as their points are clear:

We asked whether the model of Nowak, Tarnita, and Wilson (NTW), when applied to their chosen test case of eusociality, makes any important difference. Does it refute kin selection theory? Does it offer new insights? The answer to both questions is no.

I agree with that statement.  They go on (my emphasis):

Now Nowak and Allen suggest that we have misinterpreted NTW. For example, NTW did not mean that relatedness is unimportant. Instead, they only meant that if relatedness is high and held constant, other factors determine which species evolve eusociality, and that this is an issue the kin selectionists have not considered. On the contrary, it is completely obvious from Hamilton’s rule; if you hold relatedness constant, differences will be determined by variation in costs and benefits. There have also been more specific studies about synergistic factors affecting these costs and benefits. Moreover, if this is the basis for NTW’s claim that relatedness is not causal, then we have shown that NTW’s other parameters are also not causal, because when we force them to be constant, only variation in relatedness matters. Finally, this apparent concession about the importance of relatedness is perplexing, given that Nowak and Allen expend significant effort questioning the details of exactly how we modeled lower relatedness, while continuing to equivocate about the real issue of how relatedness matters. Low relatedness groups are real and can be formed in many ways, but with offspring control they do not give rise to eusociality. If Nowak and Allen think otherwise and believe that there are reasonable ways to lower relatedness so that it does not make eusociality harder to evolve, then they should show how.

This is telling. NTW truly equivocate about the notion of “causality”, using a double standard when assessing relatedness versus ecological factors. In fact, as Queller notes, both ecology and relatedness can be “causal” in the sense that, if other things are held equal, variation in these factors can both tip the balance toward the evolution of eusociality. The question is whether relatedness did tip the balance, and the results of Hughes et al. (2008) suggest that it did.

Finally, Queller et al. end their response like this:

. . . If NTW did not actually mean that relatedness is unimportant, and if they did not mean that workers are merely robotic extra-somatic projections of the queen’s genome, and if they did not mean that eusociality was as hard to evolve as suggested in their main examples, then we are in happy agreement! But if this is so, why do they not just explicitly say, for example, “our method agrees with inclusive fitness in showing that higher relatedness is crucial in the evolution of eusociality”? Perhaps because it would require admitting that what we have learned about eusociality from kin selection models still stands, and that the NTW models, despite their much greater complexity, have so far added little more.

This is as close as Queller, a soft-spoken guy who doesn’t like controversy, can come to calling his opponents misguided but ambitious scientists who won’t admit that they’ve distorted the situation. That, at least, is my take on the exchange. Nowak and D. S. Wilson have staked their careers on the “kin-selection-is-wrong-and-my-theory-is-better” view, and they’re obdurate about that. But such stubbornness is more akin to theology than to science.

 ______

Hughes, W. O. H., B. P. Oldroyd, M. Beekman, and F. L. W. Ratnieks. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213-1216.

Liao, X., Rong, S., and D. Queller, 2015. Relatedness, conflict, and the evolution of eusociality. PLOS Biology | DOI:10.1371/

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

Nowak MA and B. Allen (2015) Inclusive fitness theorizing invokes phenomena that are not relevant for the evolution of eusociality. PLoS Biol 13(4): e1002134. doi:10.1371/journal.pbio.1002134

Queller, D. C., S. Rong, and X. Liao. 2015. Some agreement on kin selection and eusociality? PLoS Biol 13(4): e1002133. doi: 10.1371/journal.pbio.1002133

 

59 Comments

  1. Griff
    Posted May 7, 2015 at 11:22 am | Permalink

    How would group selection work? What is the target for selective pressure if two organisms don’t share alleles?

    Are there any clear examples of organisms sacrificing their own ability to reproduce for another, unrelated organism?

    • H.H.
      Posted May 7, 2015 at 2:00 pm | Permalink

      Are there any clear examples of organisms sacrificing their own ability to reproduce for another, unrelated organism?

      Soldiers going off to war immediately springs to mind.

      • reasonshark
        Posted May 7, 2015 at 2:19 pm | Permalink

        Even that’s not a straightforward example. Pinker explains it more fully in his article against group selection, but the main point is that there are a lot of circumstances and caveats to keep in mind when comparing, say, an ant colony’s soldier with a human soldier.

        http://edge.org/conversation/the-false-allure-of-group-selection

        For instance, it often takes a lot of manipulation, coercion, and compensation – a huge chunk of which is cultural – to even get soldiers involved in risking their lives for other people, regardless of whether it’s done for their tribe, their empire, or their state. Never mind the paucity of human soldiers routinely and instinctively throwing their lives away to advance a higher cause. That’s precisely what you would expect if humans evolved according to the rules that come from increasing or maintaining genetic fitness.

        • nickswearsky
          Posted May 7, 2015 at 3:35 pm | Permalink

          Some of that manipulation, coercion, and such done in the military helps establish group identification. I’ve read some interesting articles on the importance of group identification in everything from nationalism to sports fans. I think once you’ve established a group identification, behaviors that favor the group and not so much the individual follow more easily.

          Hence my question below. I understand the importance of kin selection, but does that mean group selection cannot at some point factor in?

          • reasonshark
            Posted May 7, 2015 at 4:42 pm | Permalink

            I don’t think you grasp the issue here. Group selection isn’t propped up because of social instincts towards groupiness. Nor does social living have to entail individual disadvantage – especially costly disadvantage – for the genes and their hosts. There’s a wealth of reasons why some social organisms would evolve to identify with a “group” of many kinds, and why group members may sometimes be willing to take huge risks for the group at large. It’s not a vindication of group selection.

            There are reasons to think strong social instincts – even potentially self-sacrificing ones – can be co-opted in ways that differ from how and why they evolved in one’s ancestors. A good example provided by Pinker is the strong feeling of family and brotherly love that can be diverted into strengthening soldier solidarity. And in the case of humans, the picture is complicated by cultural forces with causal powers of their own, such as sweeping historic movements that people find compelling for various reasons. Even where individuals commit genetic suicide, it’s not enough. You can’t just show that it happens: you have to show that it’s a consistent, widespread, even natural thing for the organisms to do, like ant soldiers cheerfully getting slaughtered en masse for the good of the genes in their relatives and the reproducing queen. And Pinker shows that a) there’s already a superb explanation for that process in soldier ants, and b) humans as a species are not like that at all.

          • reasonshark
            Posted May 7, 2015 at 4:43 pm | Permalink

            More to the point:

            What group selection proposes is that you can apply the logic of natural selection to “groups”, especially to explain behaviours that are, in the biologist’s sense, altruistic. Kin selection, despite the similarity of the name, is not “the same, but for kin rather than groups”; it’s a precise extension of the logic of gene-centric natural selection, in which the genes and their various alleles (variations) are together the ultimate unit of selection – a replicator – and other biological entities are complex tools.

            The strength of kin selection comes from the clear contribution of the logic of genes being the targets of selection. A gene that influences its host to help hosts containing its copies is, in a sense, helping itself, so given certain cost-benefit analyses, we would tend to find organisms that behave in certain ways towards their close kin, who share the highest probability of carrying their alleles. It is most emphatically not “selection applied to kin”.

            The alleles are still the crux behind the argument. This also applies to theories of reciprocal altruism: a carrier of an allele “pays” an unrelated organism in return for a benefit.

            Group selection, by contrast, is all over the place as an attempted explanation. Its practitioners slap the “group” label on such disparate kinds of socially interacting collections of organisms that it obscures more interesting and relevant distinctions.

            I’ve met proponents who can’t grasp that, if the theory is indistinguishable from existing gene-level-selection models with actual explanations, it’s useless as a theory because it can’t distinguish noise from signal and doesn’t shed light on what’s there anyway. It fails at the replicator-vehicle distinction required to understand selection: even groups of asexual clones can’t truly replicate, and the need to make a group a vehicle requires a genetic bottlenecking to keep a “group” as a unified unit like a single organism, which so far can only be obtained by using kin selection logic anyway (such as in the somatic-gametic distinction of a single organism’s body – which is basically a colony of genetic clones – and in eusocial insects with reproducing queens and sterile workers). And this is before we get to the fact that group selection models so far haven’t yielded findings you couldn’t gather through already-established frameworks such as ESS theory and inclusive fitness.

            There are a lot more problems detailed in that Edge article I linked to, but in short: you’d go a lot further in understanding social behaviours of both non-human and human animals without once getting bogged down in the confusion, impracticality, and empirical dead-end streets that make up group selection.

            • nickswearsky
              Posted May 8, 2015 at 7:58 am | Permalink

              Thank you for the detailed answer. As I mentioned, I am not up on this topic, so I appreciate the reply. I’ll have a look at the Edge article.

    • reasonshark
      Posted May 7, 2015 at 2:07 pm | Permalink

      The only good examples I can think of off the top of my head are ones in which a parasite gets inside an unrelated host and either castrates it or forces it to commit suicide.

      I admit it’s a bit fatuous, but the flip-side of biological altruism (in the sense of a gene-carrying organism sacrificing survival and reproductive prospects to further those of another organism) seems to me to be indistinguishable from parasitism.

      In theory, a group itself could be a gene-like structure and you could imagine associated organisms replicating like DNA strands, or you could imagine organisms combining into a genuine superorganism, so that they act like one individual with an inheritance bottleneck (so that the fate of the genes of all the hosts were tied together, meaning cooperation would benefit everybody). Empirically, you might find eusocial-like behaviour patterns with no genetic or “inclusive fitness” correlation. That’s why the issue of relatedness is so important in the paper.

      The trouble is that we’ve currently got better evidence for the aquatic ape hypothesis than for group selection theory. And it is hard to imagine a plausible scenario of, say, some kind of superorganism function without invoking stronger frameworks such as kin selection, selfish gene theory, mutualism, and reciprocal altruism to do the actual explanatory work.

      • Mark Sturtevant
        Posted May 7, 2015 at 2:54 pm | Permalink

        There is social parasitism, as in where a cowbird tricks another species to raise her chicks.

      • Posted May 7, 2015 at 3:03 pm | Permalink

        The trouble is that we’ve currently got better evidence for the aquatic ape hypothesis than for group selection theory.

        We are aquatic apes. But, best I know, there’s no indication that we’ve ever been significantly more aquatic than we are today.

        b&

        • Marella
          Posted May 8, 2015 at 5:27 am | Permalink

          I loved that hypothesis, so sad its wrong.

          • Posted May 8, 2015 at 7:53 pm | Permalink

            Oh, don’t be sad! Just head down to the beach and enjoy your heritage as an honest-to-goodness actual living aquatic ape!

            b&

    • Mark Sturtevant
      Posted May 7, 2015 at 2:52 pm | Permalink

      Yes, but the ones that I think of are more like aberrations that evolved as behaviors for strong parental care via kin selection. A lioness who is still lactating but has lost her cubs might adapt a gazelle fawn and nurse and protect it (for a time). As long as she is nursing another animal she will not ovulate. There are many examples of that sort of thing where strong parental instincts, which evolved by kin selection, result in occasional instances of cross-species nurturing.

      • Posted May 7, 2015 at 5:30 pm | Permalink

        Yes. The critical thing about inclusive fitness is that it the totality of the effects that are important. A heritable trait could be maladaptive in some individuals but if this cost is outweighed by a greater benefit (to the underlying causal genetic variant) across the population as a whole, that trait will still be selected for.

  2. krzysztof1
    Posted May 7, 2015 at 11:50 am | Permalink

    “Nowak and his colleagues are showing a characteristic trait of some scientists: a complete refusal to admit that their critics had any valid points at all. ”

    Which is a trait not limited to scientists, I might add!!

    • krzysztof1
      Posted May 7, 2015 at 11:55 am | Permalink

      [But scientists should know better!]

    • Charles Jones
      Posted May 7, 2015 at 3:39 pm | Permalink

      I can cite a couple of examples of scientists who have some maverick idea that few peers accept, but in each of these examples these folks continue to find a publish evidence supporting their minority view point.

      Why haven’t Nowak et al. published follow-up studies buttressing their point of view? This seems very odd to me.

  3. JJH
    Posted May 7, 2015 at 11:52 am | Permalink

    Great post!

    As a non-expert in biology (but dang, natural selection is not a hard concept to understand), when I hear politicians and pundits discuss, “teach the controversies involving evolution”, this is the type of discussion I wish they were having!

    Added kudos, again as a non-expert, I actually understood the level of selection arguments as broken down in the post!

  4. nickswearsky
    Posted May 7, 2015 at 12:05 pm | Permalink

    Forgive my question as a non-expert. But, is it possible that kin selection is necessary for the origin of eusociality but something more like what the other describe as group selection can operate once the groups have been established?

    • darrelle
      Posted May 7, 2015 at 12:54 pm | Permalink

      Not an expert either. My understanding is that there are no selection puzzles that group selection models explain that kin selection models don’t also explain, and do so more parsimoniously. Also, there are selection puzzles that kin selection models explain that group selection models do not.

      Models = Mathematical models.

      • nickswearsky
        Posted May 7, 2015 at 1:39 pm | Permalink

        That does sound sensible. Thanks! Any experts who care to weigh in?

        • Brad
          Posted May 7, 2015 at 2:56 pm | Permalink

          Also a non-expert. I’ll volunteer a couple clay pigeons to be shot down re group selection:
          The evolution of near-simultaneous calving in herds of migratory ungulates as a defence against predation of the young. I’m thinking specifically of caribou, but this probably occurs in African grazers and others; I don’t know.
          Colony nesting in sea birds, even in the absence of effective nest defence nests in a colony would have a lower probability of predation than isolated nests.
          Long generation times with extended protected pupal/larval stage in insects such as locusts or cicadas.
          Mobbing behaviour by crows against predators of young birds such as hawks and owls.
          In these examples the individuals are not necessarily very closely related, although the groups involved would probably be more closely related than random individuals of the species. And the behaviour benefits both the individual and the group.
          A couple other examples which I think are likely kin selection are the (presumably simultaneous) evolution of toxicity and brilliant colouration in frogs and butterflies. Being toxic and brightly coloured probably reduces your individual fitness compared to being camouflaged, but if your sisters and cousins and your aunts are also brightly coloured and toxic, the net fitness of the group might be enhanced if the predator learns his lesson.

          • eric
            Posted May 7, 2015 at 3:37 pm | Permalink

            Those all seem to be examples of the “herd defense” strategy, which is adequately explained by standard evolution because it benefits the individual’s likelihood of procreation, survival, etc… It benefits the each individual caribou mother to give birth when others are doing it, because with so many calves around the odds of their particular calf getting targeted for predation goes down. It benefits the individual sea bird to nest with others for the same reason; it reduces the chance that that individual will be targeted by a predator. For the crows, attacking in a group reduces the change that individual will sustain an injury from the hawk.

            AIUI, to demonstrate group selection as a driving mechanism, you have to think of a situation where a group of critters who do not derive any individual or kin-related benefit from being in the group out-compete some other group whose members do.

            • reasonshark
              Posted May 7, 2015 at 5:00 pm | Permalink

              AIUI, to demonstrate group selection as a driving mechanism, you have to think of a situation where a group of critters who do not derive any individual or kin-related benefit from being in the group out-compete some other group whose members do.

              I think the superorganism idea is the closest one could reasonably expect. A single human, for instance, is a colony of cells, many of which will off themselves to keep the whole apparatus running and only a handful of which will proceed to the next generation (the gametes). The obvious problem is that the colony is a bunch of genetic – actually genomic – clones, so kin selection has it in the bag.

              Another is the longevity of particular ESS’s (evolutionarily stable strategies, or evolutionarily stable states for a mix of strategies that balance out). Some ESS’s will drive a population extinct, even as the population-diminishing strategies responsible are still doing well enough to persist from generation to generation. For instance, a population dominated by cheats may exploit itself to death even though cheats are the ones prospering more than other rival strategies. Other ESS’s won’t drive themselves extinct. Over the long term, we would expect to see more of the latter than of the former, simply because the former have a tendency to drive themselves extinct.

              Again, though, this is better explained without resorting to group selection theory. In fact, it’s not strictly speaking an evolutionary process, but an artefact of existing evolutionary processes. It certainly couldn’t explain how adaptations arise; all it does is point out sets of adaptations that lead to extinction.

      • Daniel Engblom
        Posted May 7, 2015 at 2:49 pm | Permalink

        Not an expert but this is my understanding as well.

    • Mark Sturtevant
      Posted May 7, 2015 at 3:04 pm | Permalink

      That does not seem a bad question at all. No expert here either, and group selection makes my head spin, but I have thought that group selection sort of resembles what humans do now. Our origins were from smaller, more related groups where kin selection would prevail. But now we live in huge societies of unrelated individuals with our genetic relatives still closest to us.
      I do not know how to parse all of this, but I wonder if there was something worth while in there somewhere.

      • eric
        Posted May 7, 2015 at 3:43 pm | Permalink

        I think humans are often in the case where some group rule or social practice benefits the individual’s chance of successfully passing on their genes. Which is not group selection. Simple example: “Don’t kill” laws may prevent me from killing a rival suitor for my preferred mate, but if I’m going to find another mate anyway and it prevents me, my mate, or my offspring from dying, then this is not group selection for groups with “don’t kill” laws, its just normal selection.

  5. Pascal Nelson
    Posted May 7, 2015 at 12:25 pm | Permalink

    Very interesting and clearly done, PCC. I read this post with interest and comprehension. It really helped me to understand the issue of kin selection.

    Also, it illustrates the workings of scientific discourse.

  6. Posted May 7, 2015 at 12:39 pm | Permalink

    A quick read-through was enough for me to get the gist, but I’m going to have to circle back later today for a re-read to fully digest it…once again, curse you for making me have to think!

    b&

  7. Posted May 7, 2015 at 12:59 pm | Permalink

    Thank you, very interesting.

    When I read The Selfish Gene I was so struck by the idea that is seemed like a revolution (in my small mind). it seemed to clear and correct — much like evolution by natural selection itself.

    Seems to me that if you think about these things carefully, the result is inevitable.

    But, I hold no degrees in the field of biology, so who am I to comment? 🙂

  8. Posted May 7, 2015 at 1:00 pm | Permalink

    Thanks, Jerry, for keeping us up on the latest developments in this bizarre controversy. I second your astonishment that Nowak and the two Wilsons are doubling down instead of acknowledging the importance of kin selection.

  9. Mark Sturtevant
    Posted May 7, 2015 at 1:31 pm | Permalink

    I have learned that eusociality is seen in a fair variety of organisms, including aphids and thrips. Eusocial aphids might provide a relatively simple way to test these ideas on a large scale.

  10. Darwinian Demon
    Posted May 7, 2015 at 1:41 pm | Permalink

    “On the contrary, it is completely obvious from Hamilton’s rule; if you hold relatedness constant, differences will be determined by variation in costs and benefits.”.

    Very well put!

  11. Daniel Engblom
    Posted May 7, 2015 at 1:49 pm | Permalink

    Another great article 🙂

  12. Delphin
    Posted May 7, 2015 at 3:24 pm | Permalink

    Hard sledding, so thank you. I’d never get this from any other source.

  13. Christian Giliberto
    Posted May 7, 2015 at 3:34 pm | Permalink

    To open with a cliché, long-time reader, first-time commenter. I want to thank PCC for the continuing, excellent coverage of this whole controversy. As an undergraduate taking evolutionary biology as we speak, the science posts here are some of my favorites. They’re really helpful pedagogically.

    Just from my student’s-eye-view, it was news to me that inclusive fitness was such a “limited concept,” as NTW claimed in their April 24th PloS piece, given how many successful examples of the kin selection approaches we’ve gone over in class. That piece at least felt like bizarro world when compared to the papers about social behavior/biological altruism we’ve been reading (e.g. about mating coalitions, models of alloparental care, etc.) where -often successful- use of inclusive fitness seems fairly ubiquitous.

    Thanks again, great post!

  14. Josephine
    Posted May 7, 2015 at 3:47 pm | Permalink

    Commenting, even if only to add one more comment to a nice biology post. Otherwise a long-time reader, who finds this website immensely enlightening.

  15. Posted May 7, 2015 at 5:02 pm | Permalink

    Nowak and Allen also note (see their Figure 1), that among the many species that have the kind of mother/offspring association that could promote eusociality (“progressive provisioning,” in which offspring are continuously fed in nests), only a few have evolved eusociality.

    Seriously? Isn’t that just a fancier way of saying, “if evolution is true, why are there still monkeys?” Or, “if XYZ drives evolution towards larger body size, why are there still small animals?”

  16. eliz20108
    Posted May 7, 2015 at 5:05 pm | Permalink

    Keep writing these scientific blogs. I understand about one in 1000 ideas but I want to learn.

    Thank you for your effort.

    I have a PhD in sociology, minor in statistics.

  17. Posted May 7, 2015 at 5:25 pm | Permalink

    I know it’s not a very scientific argument but kin selection (and inclusive fitness) just makes so much sense – I find it hard to see how it can NOT be important.

    Overall, this seems like the old chestnut of inflated significance:

    A: “X is important.”

    B: “Ah, but X is not the ONLY important thing. You also need Y.”

    A: “True.”

    C: “Therefore X is not important.”

    A: “Um, what?!”

    • aspidoscelis
      Posted May 7, 2015 at 7:31 pm | Permalink

      An analogy: To bike to work, you need a bicycle. Suppose you’re looking at a group of people and want to know why some bike to work and some don’t. They all have bicycles.

      Is bicycle ownership an important factor in answering your question? Nope.

      • Posted May 9, 2015 at 7:41 am | Permalink

        Under your analogy, Nowak et al were only asking people whom they already knew had a bike. Nothing could therefore be said about the importance of bike ownership. If they just asked a group of people without that constraint, it might indeed turn out that owning a bike was important.

        • Peter Nonacs
          Posted May 9, 2015 at 8:57 am | Permalink

          To be fair on this analogy, what Nowak et al are criticizing would be their perception that sociobiologists believe the only way to get to work is on a bike (by showing that even with a bike, some people don’t go to work!). But this is a gross exaggeration on the thinking in the field. It would be more accurate to say: “There are a number of ways to get to work, but it can be really helpful to have a good bike.” Nowak et al never address the ‘how helpful’ part, which is what the response paper does.

          • Posted May 9, 2015 at 7:19 pm | Permalink

            As written, though, that’s just bad logic along the lines of: Dogs have four legs. My cat has four legs. Therefore my cat is a dog.

            No one was saying that the relatedness required for kin selection always results in eusociality. (Were they?!) Something can be necessary but not sufficient – and still be very important as a result. Nowak et al just show that it’s not the _only_ important thing.

            • Peter Nonacs
              Posted May 9, 2015 at 8:00 pm | Permalink

              No, but as many read Nowak et al saying relatedness is unimportant (when they don’t actually say that, although it is easy to get that impression), there is lot out there in the literature by kin selection advocates that seems to say you can get to eusociality only THROUGH high relatedness (i.e, it is a necessary preadaptation). Although again, they may not explicitly say that, it is easily read that way.

  18. Posted May 7, 2015 at 6:12 pm | Permalink

    I’m weak on the biology portion, but causality is of particular interest to me. Nowak, et al. say,

    “Whether or not eusociality evolves depends on the demographic parameters of the queen (…), but not on relatedness. The relatedness parameters would be the same for all species under consideration”

    As already mentioned, it seems highly unlikely that the relatedness parameters would be completely fixed (really, what’s a single example of an animal society where that is the case?). But even if we completely granted them this, I still don’t see how they can claim that this implies no causal effect of relatedness on the evolution of eusociality.

    As an analogy, suppose I claimed that humidity plays no causal role in the event of rain, at least when we fix the humidity level at, say, 70%. Rain is actually caused by other factors like pressure and air temperature. But I still need to compare what happens when humidity is at some other level, all else fixed, in order to make a causal claim. Most naturally, we would look at 70% vs. 0% humidity. But rain is certainly more likely to occur at the 70% level than the 0% level of humidity; therefore, humidity does have a causal effect on a rain event.

    I don’t see Nowak, et al. ever doing anything like this. They seem to just say relatedness is noncausal by fiat. But would the chance of eusociality evolving stay fixed in a population with zero relatedness? That seems highly unlikely. So even if the models of Liao, et al. don’t actually appear often in nature, that doesn’t mean they don’t say something about the causal nature of relatedness to evolution of eusociality. 0% humidity doesn’t occur in nature either, but comparing its effect on a rain event to 70% humidity does indicate a causal element.

  19. aspidoscelis
    Posted May 7, 2015 at 7:22 pm | Permalink

    My $.02: If eusociality can or has evolved when variation in relatedness is not the primary factor, group selection wins. Kin selection is a special case of the general group selection framework; in order for group-level traits to emerge within a species, there must be some factor causing groups to be cohesive enough that they can act as units of selection. “Group selection” is the position that this can happen; “kin selection” is a more specific claim that, yes, this can happen–but relatedness is the -only- factor that can be involved.

    So far as I can tell, holding relatedness constant in the NTW model is based on their belief that this is an accurate depiction of the conditions under which eusociality evolved (non-eusocial species with groups of individuals that share high relatedness evolved first; some subset of these non-eusocial species became eusocial; ergo, the transition to eusociality post-dates the origin of high-relatedness groups), not on an a priori rejection of relatedness as a potentially important factor in the evolution of eusociality. I have no idea whether or not the NTW scenario is accurate, but my interpretation of their paper is that high within-group relatedless may be a necessary precondition for the evolution of eusociality, but is not sufficient. The model, then, is intended to look at what further factors actually lead to eusociality once that precondition has been met.

    I haven’t read the paper recently, I should probably re-read it. My recollection is that the TL/DR version is: It ain’t just relatedness, folks.

    • Gregory Kusnick
      Posted May 7, 2015 at 10:27 pm | Permalink

      I don’t see kin selection as a special case of group selection, and I don’t think most biologists do either. There’s nothing in Hamilton’s rule about group cohesion.

      All that’s needed for kin selection to operate is some mechanism by which individual organisms can plausibly estimate their degree of relatedness to other individuals. That can happen even in the absence of clear-cut groups — something that can’t be said for group selection with its emphasis on the group’s gene pool as a unit of selection.

      • aspidoscelis
        Posted May 8, 2015 at 8:47 am | Permalink

        I’m aware that most biologists don’t see kin selection as a special case of group selection. However, I am not part of that “most”. 🙂

        So far as I can tell, NTW and the other current advocates of group selection aren’t, either. This makes criticisms of them for rejecting kin selection somewhat confusing; to the extent that they reject kin selection in favor of group selection, so far as I can tell their intent is to reject the ideas that relatedness is the only factor that can lead to selection above the level of the individual and that all group-level phenomena must be reframed in individual-level terms.

        Regarding this: “All that’s needed for kin selection to operate is some mechanism by which individual organisms can plausibly estimate their degree of relatedness to other individuals.” In practices, that mechanism is shared group membership, I think. At least, that seems to be the case in the examples I’m somewhat familiar with (mostly insects). However, I’m not sure it would be a problem for group selection if it worked the other way around (group membership inferred from a direct estimate of relatedness). It’d be a fun mental exercise to work through that…

        • reasonshark
          Posted May 8, 2015 at 10:06 am | Permalink

          so far as I can tell their intent is to reject the ideas that relatedness is the only factor that can lead to selection above the level of the individual

          But that way of framing the debate isn’t even remotely correct to begin with.

          Kin selection isn’t about “selection at the level of families”. It’s an explanation for why some organisms are nepotistic in certain ways, and it’s an explanation that makes use of the gene-centric theory of selection. Ask a kin selectionist for whose “good” those adaptations are for, and they will reply “for the ‘good’ of the genes”, not “for the good of the family”. This is the opposite of what group selectionists would say; they’d say – and have said – that particular social adaptations arise “for the good of the group”.

          Heck, individual selection isn’t technically correct either, though it’s a convenient shorthand because the interests of the alleles and the interests of the individuals often coincide (neither “want” to get eaten, for instance). Individuals are collections of phenotypes which alleles use to “win” their chances at replicating and going to the next generation, and those phenotypes persist because the associated genotypes persist.

          That’s simply because individuals don’t actually get copied per generation: if a cloning aphid lost a leg, its descendants won’t inherit the leg loss, simply because they’re really inheriting the genetic code that influences the growth of legs. And even cloning aphids are basically colonies of cloned cells that cooperate like a chess team (with some strategic sacrifices) to get their alleles into the next generation. While the traits of an individual can be selected for the next generation, and so one could talk about individual selection in that sense, it’s ultimately got a gene-selection rationale behind it. As with bodies, so with nepotism.

          Granted, you can look at the big picture and describe non-random patterns in social species, such as what traits or adaptations would arise and prosper in organisms that gather and associate. One great example is the concept of the ESS (evolutionarily stable strategy, or evolutionarily stable state for when many strategies can coexist). And a particularly interesting thing about ESS is that some types of ESS are more likely to lower the average payoff of or even drive to extinction the population at large.

          A good example is in The Selfish Gene: in the game setup by Axelrod, Always Defect and Tit For Tat were two strategies that could gain dominance and potentially qualify as ESS’s, but the nature of Always Defect was that a population of them would do each other in and diminish the total payoff, whereas Tit For Tat could survive on runs of mutual cooperation and so last longer than Always Defect. The catch is that, in the Always Defect population, no strategy can do better at any point during the collapse because Always Defect is still an ESS, and so no rival strategy can do better against it.

          This is fascinating and insightful material, and there’s even a resemblance to group selection. But the fact that one ESS may drive a population extinct (whereas another won’t) doesn’t require an analogy with selection, as if there were some higher-order selection process favouring the latter.

          It doesn’t work in reverse: Tit For Tat won’t be selected because of its population-preserving properties. It’ll be “selected”, if anything, for the same reasons Always Defect would be “selected”, with the eventual fate of the population being an artefact of that “selection” (a side effect that might explain why we don’t see many Always Defect populations). And I put quotation marks around “selection” because it’s just a word of convenience. What would really be selected would be the alleles that contribute to the embryological processes that produce the phenotype that, among other possible effects, inclines an organism to follow that particular strategy.

          A bit unwieldy, perhaps, but the gene-centric nature of the selection is still key. And that’s why kin selection is not a special case of group selection: it has nothing to do with “other levels of selection” and certainly not, despite the similarity of the name, selection of kin themselves.

          • reasonshark
            Posted May 8, 2015 at 10:07 am | Permalink

            P.S. Also, group selection isn’t vindicated just by indicating group identification and membership. I won’t repeat my response to this point when nickswearsky brought it up further up the page, but suffice it to say that there are plenty of ways to describe and explain how social organisms form coalitions without once invoking group selection.

      • Peter Nonacs
        Posted May 8, 2015 at 2:31 pm | Permalink

        Nowak & the two Wilsons tend to intertwine two issues. For the Wilsons it is the relative effect of group versus kin selection. This argument can seem pointless because kin effects can happen only between multiple individuals (i.e., within a group), and to understand across-group selection, you need to also specify within-group kinship levels (and this is particularly important as to how DS Wilson’s structured deme group selection models will work). Thus for many it is simply a terminological debate, and one should use whichever point of view works best for analyzing a particular situation. If groups form on the basis of admitting or rejecting potential members by relatedness, then kin selection is the more obvious method. If groups randomly vary with respect to kinship, then group level selection models are what you need. But for Nowak, the bee in his bonnet is mostly the widespread use of inclusive fitness models to predict the course of evolution, primarily as exemplified by Hamilton’s rule: rb > c for cooperation to be favored. It is truly not whether kinship is irrelevant. Thus, Nowak favors a more general mathematical approach that encompasses both kin and group effects, where you basically ask: if trait X produces effect Y, will the trait spread in the population? This is a more substantive criticism and one actually needs to be careful about the type of question one asks. For example, Hamilton’s rule is accurate in predicting that if an individual has a choice and can only help a full sibling OR a half sibling, that help should go to the full. However, if you ask a population-level question such as “would cooperation spread faster if parents were always monogamous (producing offspring who are all full sibs), rather than polygamous?” – Nowakian type of population models show there is no particular advantage to monogamy. I think Nowak goes way overboard in wanting to dump inclusive fitness completely, but one needs to apply IF reasoning carefully and Hamilton’s rule can be too simple to apply universally.

      • Posted May 9, 2015 at 7:36 am | Permalink

        “All that’s needed for kin selection to operate is some mechanism by which individual organisms can plausibly estimate their degree of relatedness to other individuals.”

        I don’t think that even that is needed. As long as the phenotype preferentially benefits kin, I’m not sure that actual estimation or recognition is required. (Perhaps this is just a semantic issue, though. I guess it depends how one defines kin selection. Ditto inclusive fitness.)

  20. Posted May 7, 2015 at 8:49 pm | Permalink

    What I wonder about regarding the folks who say group selection is the cause of human altruism is this: Are there still groups of humans competing and reproducing at different rates? If yes, who are these groups? Are some demonstrably more altruistic than others? If not, are we now one big group, and wouldn’t individual selection now be working against the altruism instilled in us by group selection? Doesn’t the theory predict that if/when we become one big interbreeding group, we will gradually just get more selfish and less altruistic? Do they really believe that?

  21. keith cook or less
    Posted May 7, 2015 at 9:26 pm | Permalink

    As a non expert, kin selection was a real revelation when I first encounted it, a very elegant solution to a biological puzzle. In fact, I wasn’t even aware of eurosociality, let alone it being a problem. It is a pity that it still is a problem for some and I wonder if this is not a case of expert blindness.

  22. Amelia
    Posted May 8, 2015 at 4:20 am | Permalink

    Hi,

    I’m currently doing my final year exams for a degree in Zoology and we cover Nowak et al’s paper when discussing the evolution of eusociality. I’ve noticed it was an extremely controversial paper! My lecturer has looked at Nowak et al’s 4th step (emergent traits caused by the interaction of group members are shaped through natural selection by environmental forces) which involves fighting between groups and interpreted it as meaning that social animals such as lions, wolves and even humans who fight in groups as being eusocial or at this 4th step of eusociality. What are your opinions on this? And what would you summarise as the main criticisms against this paper and main evidence supporting kin selection as an explanation for how eusociality evolved?

    Thanks,

    Amelia

  23. Posted May 8, 2015 at 7:04 am | Permalink

    Two papers that may be of interest -thisfrom the autumn
    Evidence of group selection shown in social spiders
    Bryony Jones Nature Reviews Genetics 15, Pages:
    778–779(2014)DOI: doi:10.1038/nrg3851
    http://www.nature.com/nrg/journal/v15/n12/full/nrg3851.html

    &
    Good for the group? Explaining apparent group-level adaptation
    Isabel M. Smallegange*, Martijn Egas 2015 doi:10.1016/j.tree.2015.04.005
    http://www.sciencedirect.com/science/article/pii/S0169534715000956

    • reasonshark
      Posted May 8, 2015 at 10:22 am | Permalink

      The first one is fascinating, in that it would be an excellent example of how Evolutionarily Stable States fare in different environments. Presumably, the ESS for a particular colony arises in response to local conditions that are constant over multiple generations, so colonies moved to an environment that favours a different ESS would not fare as well as those that follow a locally optimum ESS. It’s a pity they don’t go beyond two generations, or it would be interesting to see if the ESS shifted over time to better match local conditions… assuming, of course, that they didn’t do an Always Defect and succeed themselves into extinction first.

      It would also be interesting to know if the correlation between colony ESS’s and their neighbours’ ESS’s was a result of environmental conditions or if the members somehow copied others until they fit in, especially since the authors admit that genetic influence would be a big factor. Lastly, it would be fascinating to know if Anelosimus studiosus colonies contain many kin and mutual gains between non-kin. Relatedness and member cooperation would likely play large roles in directing the ESS ratios.

      As evidence of group selection in the wild? They’re not even close to ironing out the confounding factors, never mind presenting anything that can’t already be explained by conventional mechanisms. I mean they admit themselves that it’s probably genetically influenced. What good’s a different level of selection if you can’t separate the signal from the noise of gene-centric levels of selection?

      If this research is considered the benchmark for demonstrating group selection, I’m not yet impressed.

  24. Diane G.
    Posted May 9, 2015 at 1:49 am | Permalink

    Great post, most appreciated!


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