A phenotypic view of evolution Evolution in Structured Populations

Wynne-Edwards, Theoreticians and Group Selection: When Data Meets Theory

When talking about multilevel selection it is worth giving a bit of history.  This does two things.  First, it shows us where we came from, but more importantly, the study of MLS is fraught with missteps that perhaps we can avoid in the future. . .

In talking about MLS one should probably go back to Darwin and his pondering about sterile casts in insects; however, the start of the modern controversy can trace back to V. C. Wynne-Edwards, and that is where I will start.  Wynne-Edwards, like many fine biologists of his time, was first and foremost an exceptional naturalist.  What he knew best were the Arctic pelagic birds.  Apparently he got free tickets on the Canadian Pacific line and the Cunnard line, and made several trips to Europe and back watching the pelagic birds.  He also did a number of expeditions into the deep north (Mark Borrello has a good account of this ).  What he noticed was that over fishing could occur, but those occurrences were rare, and speculated that some form of group selection was preventing that from happening.  Theoreticians – read Maynard-Smith and Williams – quickly jumped all over this and explained in no uncertain terms, that while group selection could happen, theory indicated that the chances of it being important were vanishingly small.

Wynne Edwards Baffen Island Wynne Edwards

Wynne-Edwards on Baffen Island, and later in life.

This is a story we have heard many times before.  A naturalist has an idea about how nature works, but does not have the theory to back it up.  Theoreticians then trot out the standard models and show why the naturalist is wrong.  The one I am most familiar with, besides Wynne-Edwards, are Mayr and Carson arguing for genetic revolutions.  It was a cheap and easy put down to use the models of the time to show that population bottlenecks weren’t evolutionarily important.  Perhaps the best showcase of this controversy is the interchange between Carson and Templeton on the one hand (1984. Ann. Rev. Ecol. Syst. 15: 97-131) and Barton and Charlesworth on the other hand (1984. Ann. Rev. Ecol. Syst.  15: 133-164).  In that interchange Carson and Templeton lack any formal theory to back up their claims, and are quickly outmatched by the theoretical canons of Barton and Charlesworth.  As my previous blog entries hint, the problem was not in the naturalists insights, but in the theoreticians models.  The point is, it happens all the time.

In the past, theoreticians did not like group selection, and this bias has continued to this day.  For example, Coyne, in a 2012 blog entry  makes the same hackneyed arguments that were made back in the early 1970s.   I find this stunning.  It seems to me that you ignore the masters at your own peril.  The people who are supporting group selection (and founder events) are people with their noses in the dirt studying the organisms. They KNOW the biology of their organisms, and by-in-large when they have a strong opinion about their study organism they are very likely at least mostly right.  On the other hand the theoreticians that are complaining have a bunch of mathematical gibberish that few understand (I know, I am one).  They are complaining about a master’s knowledge of a system that they have never seen.  So, here is my first adage:

When a good naturalist has an insight that does not agree with your world-view do not dismiss that insight until you truly understand it.

I know nothing about Wynne-Edwards’ pelagic birds, but I do know that he was an excellent naturalist.  If he says there is group selection I am inclined to believe, while he may not be right, but he is probably not wrong.  By that I mean he is almost certainly correct that something important is going on, but he may not be exactly correct as to the mechanism.  In short when a dirty fingernails biologist sees a pattern that does not fit with theory, theoreticians should ask themselves what is wrong with their theory.  Instead they seem more inclined to tell them that they are “just a naturalist” and if they listened to the theory instead of the organisms they would understand why they were wrong.

Of course it gets worse than that.  It was soon readily accepted that group selection was unlikely to be important, a view nicely captured by Harrison and Hastings in 1996 (TREE 11: 180-183):

“. . . extinction and recolonization have only a limited potential to create, or coexist with, strong genetic differentiation . . ..  This implies that adaptive evolution is unlikely to occur by classic interdemic selection, a conclusion that has often been reached.”

Into this mix comes Michael Wade.  His advisor was Thomas Park, another fine naturalist, but a laboratory naturalist.  Park spent his career working with Tribolium flour beetles.  One of the results of his work was that in just a few generations he was able to get three strains of Tribolium confusum, one with a large, one with a medium and one with a small population size.  When raised in the same conditions the large population size strain had a ten-fold larger population size than the small population size strain.  Park was an ecologist, so he focused on the ecology of why these strains had such different population sizes.  After much work he showed that the differences were due to cannibalism rates (Park, Mertz, and Petrusewicz 1961. Physiol. Zoöl. 34: 62-80).


Tribolium confusum

Given his work with Tribolium, it is hardly surprising that he was open to Wade doing an experimental study of group selection.  Note that here is an experimentalist and naturalist (Park), with his knowledge of Tribolium biology, learning about the group selection theory with his graduate student, and deciding that the two are not in agreement.  Here the experimentalist is at a huge advantage over the theorist,  since they do not need to work from the old theories.  Does group selection work?  They decided to try it and find out.  The resulting thesis resulted in one of the classic studies of group selection (Wade, M. J. 1977. 31: 134-153)

Without going into details, Wade got a much greater response to selection than he expected.  Since that time there have been numerous studies that have confirmed that group selection is much more effective than anybody would have believed (Goodnight and Stevens 1997. Am. Nat. 150(Supplement): S59-S79).  Yet, the majority of evolutionary biologists, and a lot of theoreticians, dismiss group selection as being ineffective.  This has the makings of a theoretician’s dream.  We have experimental results that are at odds with the theoretical predictions.  This is ripe for asking why the old models don’t work.  So this brings us to my second adage:

When data and theory disagree it is the theory that is wrong.

For reasons that are not clear to me, even though experiments show that group selection is surprisingly effective over a wide range of conditions, it has not garnered theoretical attention among evolutionary biologists.

Wade Results


Wades results.  Red line:  Group selection for large population size, Blue line:  Group selection for low population size.

In any case to sum up this essay (rant?) I think the real problem is that biologists, and especially theoreticians, are like everybody else: They have their own preconceived ideas about how the world works.  When presented with data that disagrees with those views the first reaction is to either ignore or dismiss those data.  However, the truth is that there is gold in those disagreements, for it is reconciling inconvenient data with our world-view that real advances are made.

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  1. Philosophers of science would now probably say something about observations being theory laden. For example, what is to be made of epideictic signals? Wynne-Edwards does not simply observe birds flying in flocks, but he sees birds signaling population density. His theory influences his observations.

    From my trials at reading Wynne-Edwards I got the impression that his big tome is like Frederic E. Clements’s. It is a thicket of jargon we no longer use and it would require an immense deal of thinking oneself into that explanatory system in order to decode it.

    What remains, then, are a few theoretical passages that can be decoded still. But even that is usually not done properly (see posts on Wynne-Edwards at my blog).

  2. Joachim:

    Thank you for your much better insight into this than I have.

    I am inclined to agree that Wynne-Edwards was naive in his conception of group selection, and his idea of treating it as essentially population level physiology is probably not an analogy that we would accept today.

    That is always the tension between natural history and theory. Natural historians tend to have a theoretical naivete that is equaled by the biological naivete of theoreticians. The problem is that we tend to give more credence to theory, when instead we would probably be better served by acknowledging that natural historians often have excellent intuitions about how evolution is working.

  3. Some sympathetic but nitpicking comments:

    1. Williams was a naturalist as much as a theoretician. He took offense with Emerson’s lectures on eusocial insects first. Citations to Wynne-Edwards were, if I remember his 1996 preface correctly, added late.

    2. We do not celebrate Darwin more than, say, Buffon or Lamarck for all his observations but for coming up with the correct mechanism of natural selection. I agree here, that rejecting Wynne-Edwards’s theory should be distinguished from his observations or from rejecting group selection in principle.

    3. Wynne-Edwards (1962, p. 13) regarded populations as homeostatic systems and wrote:

    “In the balance that we are considering here it is postulated that population-density is constantly adjusted to match the optimum level of exploitation of available food-resources; and as food-supply ‘futures’ change with the changing seasons the population-density must be adjusted to match–in so fas as this is possible in existing circumstances.”

    That’s a machine or super-organism metaphor for the population (group). I guess you will not agree with this conception of groups as supra-individual entities with their own ‘physiology’ so to speak?

    Taken in its own terms Wynne-Edwards’s theory remains false, IMHO, no matter how correct his observations were or how valid multilevel selection theory now is. Trials to vindicate Wynne-Edwards in retrospect, seems like saying that Lamarck was correct after all, because Darwin showed that evolution can work after all.

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