A phenotypic view of evolution Evolution in Structured Populations

Gardner’s theory of multilevel selection 3: the discussion

This week I will finish up with Gardner’s paper (2015 Jour. Ev. Biol doi:10:1111/jeb. 12566) which I have been discussing for the past two weeks. Given the problems with the literature review and the model, it is hardly surprising that this has led to issues with the discussion. I have problems with virtually the entire discussion; however, I will focus on the ones that I find most concerning.

First, Gardner talks of collective fitness 1 vs collective fitness 2 In doing this he continues and deepens the confusion he started when he developed the model. As I make clear in my chapter on defining the individual (Goodnight 2013, Chap. 2 in “Defining the individual” Bouchard & Hueneman eds), whether you are talking about group selection 1 or groups selection 2, or for that matter group selection 10 (there is no such thing), depends entirely on the level at which you, the investigator, assign fitness. In the example Gardner gives, Group A has 12 daughters in 4 groups of 3, whereas Group B has 12 daughters in 3 groups of 4. In this example, If you assign fitness at the level of the individual organism, and presuming no other variation, the individuals in groups A and B have equal fitness. If you assign fitness at the level of the group Group A has higher fitness than Group B. The difference, of course, is that in the second instance you have a within group “developmental” process that results in different group sizes, however since fitness is assigned at the level of the group you cannot call it selection or even evolution. The problem is that with fitness assigned at the level of the group there can be no variation in fitness within groups, and thus no evolution. This leaves the question of whether it is better to assign fitness at the level of the group or the level of the organism. This is an issue that that I address in my chapter. For fairly deep philosophical reasons it basically cannot be resolved, but as long as we are clear on where we assign fitness it is not a problem. Gardner is right that this was an important issue, but it is not a conundrum. It is one that has been resolved, and no longer presents a serious conceptual issue.

However, what I find most disturbing in this section is so jaw-droppingly silly it causes me to question whether the paper is supposed to be satire. To quote Gardner:

“Cancer is often conceptualized as involving a tension between different levels of selection, with cancerous tissues achieving higher reproductive success at a within-organism level and cancerous individuals suffering lower reproductive success at a between-organism level. However, somatic tissues – including cancerous ones – do not generally contribute genes to distant future generations, on account of the demise of their lineages upon the death of the organism. Consequently, cancerous tissues do not have reproductive value, and so their proliferation within the organism cannot correspond to selection in the strict sense of the genetical theory.” (page 6, citations removed)


Seriously? You actually believe that? ( from http://www.calgaryunitedway.org/socialvoice/wp-content/uploads/2012/10/jaw-drop.jpg )

This is basic introductory evolution material. Here is the Intro Bio version: Lewontin in his article in Annual reviews (1970, Vol 1 page 1) tells us that three things are necessary and sufficient for evolution by natural selection to occur. These are:

  • There must be phenotypic variation.
  • There must be differential fitness of different phenotypes
  • The phenotypes must be heritable.

To remind you, necessary and sufficient means that you need all three, and if you have all three evolution by natural selection will occur. So, lets think about cancer. (1) is there phenotypic variation? Yes, Cancer cells are different than normal cells in many respects ranging from physical appearance to changes in the regulation of the cell cycle. (2) Are these phenotypic differences associated with fitness? Yes. For example disregulation of the cell cycle causes cancer cells to divide more rapidly than normal cells. Cell division is reproduction. Reproduction is fitness. Yes, there is variation in fitness associated with phenotype. (3) Are these variations in fitness heritable? Yes. Most, if not all, cancers are due to at least one, and usually five or more mutations. These are genetic mutations that are passed on to daughter cells during cell division. Thus, we see that in a organism with cancer we have phenotypic variation, variation associated with fitness, and the fitness is heritable. Either Lewontin is right and Gardner is wrong, or vice versa. I am going with Lewontin being right. Yes, cancer’s “. . . proliferation within the organism cannot DOES correspond to selection”

To see how silly Gardner’s stance is, consider the Wake Island rail, a cute flightless bird that did very well until World War II. On December 23rd, 1941 the Japanese occupied Wake Island, and by the time they were expelled on September 4th 1945 the Wake Island rail was extinct. Apparently the Japanese ate them when they were placed under siege by the American military. Now the question: At some point it was safe to say that the rails did “not generally contribute genes to distant future generations” and thus “. . . their proliferation . . . cannot correspond to selection . . .”. My question is when should we consider differential survival and reproduction of Wake Island rails to no longer be selection? Was it selection in 1939 before the war? How about 1941 when the Japanese invaded? Or how about the January of the likely year of their extinction, 1943? The ridiculousness of making this judgment should be obvious. Selection doesn’t see the future and neither should we when we are identifying something as selection.

wake Island Rail

At what point did differential survival and reproduction stop being selection for the Wake island rail? ( From http://www.extinct-website.com/extinct-website/product_info.php?products_id=409 )

My goal in this is to make the important point that very smart people have thought very hard about evolution. It behooves us to know what the masters said. This does not mean reading every single paper that Lewontin ever published, but it does mean not making obvious errors in logic that have been resolved by people smarter than you and I.  It also does not mean you can’t disagree with the masters.  Science advances when old paradigms are overturned.  But it does mean if you are going to disagree with the canon you should know why you disagree, and be able to defend your position.  Again, ignorance of the literature is no excuse.

With that lapse of good sense out of the way, and ignoring MLS 1 VS MLS 2 – Been there, done that, got the tee shirt – lets move on to the units of selection. Basically the first half of this section is un-interpretable gobble-de-gook that comes from trying to force Gardner’s class structure model on to the Price equation. As I said earlier, his approach is rather clutzy, but it will work as long as there is no group selection. To add group selection you MUST turn to a multivariate approach, or make the assumption that everything is additive always, and there are no interactions of any kind. In short, it simply does not work for multilevel selection in the real world. What caught my eye, however, was his example were a wasp lays two eggs a male and a female, and males and females are reasonably being treated as different classes. He is stumped by how to use a multilevel selection approach to study this. It is actually dead easy. Each individual has a male trait or a female trait (depending on their sex) and one or more contextual traits. The contextual trait is some measure of the characteristics of the group. Note that there would be a separate phenotypic covariance matrix for males and females, but a single genetic covariance matrix for the population (Lande 1980 evolution 34:292; Goodnight et al 1992 Am. Nat. 140:743). That is, with contextual analysis, there is no problem.

So here is my opinion on this and I want to emphasize it is only my opinion. I think that Gardner has an agenda. I think that agenda is that he does not want multilevel selection to be seen as a valid research program. To this end he is willing to ignore an entire literature, to be apparently willfully ignorant of quantitative genetics, to ignore the writings of such luminaries as Richard Lewontin, and to choose not to see obvious solutions. The problem is that his agenda has clouded his vision, allowed him to use sloppy thinking and logic, and to write things that are regrettable, and frankly wrong. This does not advance science. It creates noise that interferes with people who are actually trying to understand nature. I hope I am wrong. Gardner is a good theoretician, and the world needs people like him. Hopefully this paper is simply the unfortunate type of mistake we all make, and he is really working to advance our understanding of science rather than undermine a field that he doesn’t understand.

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  1. We would like to thank you once more for the stunning ideas you gave Janet when preparing her own post-graduate research and also, most importantly, with regard to providing the many ideas in one blog post. Provided we had known of your web site a year ago, we’d have been kept from the useless measures we were employing. Thank you very much.

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