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