Gardner’s theory of multilevel selection: Where he goes wrong and why

Two things have happened recently. First, Jonathan Pruitt and I (Pruitt and Goodnight 2014 Nature 514:359) have been asked to reply to a goodly number of letters to the editor concerning our paper on multilevel selection in Nature. These letters have made it clear to me that many people have a very basic misunderstanding of multilevel selection. Second, I was made aware of a recent paper by Andy Gardner (2015 Jour. Evol. Biol. doi: 10.1111/jeb.12566), which is impressive in the depths of  misunderstanding of multilevel selection that is in the paper. I have never met Andy, but I do know he is well established, and he can stand a little criticism from me. Thus, I thought his paper would be perfect for highlighting some of the very more serious misunderstandings people have about multilevel selection. There are so many problems with the Gardner paper that it will take me several weeks to work through them, so on that note, lets take his paper and start turning it into confetti. You have actually seen the opening salvo in my post last week about Fisher’s fundamental theorem. What brought that up was Gardner suggesting that the fundamental theorem was somehow special, or that it applied only to a specific subset of biological entities.

What I want to talk about this week is an idea that Gardner puts out nicely in the first sentence of the abstract: “The theory of multilevel selection (MLS) is beset with conceptual difficulties.” The truth is that MLS is in fact a mature theory. One that, at this point, has very few conceptual difficulties. We know group selection works, we know why it is so effective, we know how to extend quantitative genetics along several different pathways to incorporate the interesting results of group selection experiments, and we know how to measure MLS in the field. Finally, MLS methods are widely used in agriculture – your breakfast this morning may well have been dependent on MLS theory. Eggs, bacon (hogs) and toast (wheat) are commonly or exclusively selected using MLS methods. It is a mature settled theory, sure there is much to be done, but isn’t that true of all science?

So, why is Gardner so wrong? Well that can be seen in the first sentence of his introduction (Do you start to see why this might take a few weeks!): “Recent years have seen a resurgence of interest in the theory of multilevel selection (MLS: Price, 1972a; Hamilton, 1975; Sober & Wilson, 1998; Keller, 1999; Okasha, 2006; Wilson & Wilson, 2007; West et al., 2008; Gardner & Grafen, 2009; Leigh, 2010; Nowak et al., 2010; Lion et al., 2011; Marshall, 2011; Frank, 2012a, 2013).” What you should notice is that there are no serious multilevel selection experimentalists on this list, nor is there anybody on that list who I would call a true MLS theorist. I will not go through the list of why these people are inappropriate, other than to say that some are very old, many are philosophers, and many are advocates of kin selection, or for other reasons really should not be considered authorities on multilevel selection. One has to question where are (to list only modern authors) Wade (1977 Evolution 31:134, Wade et al 2010 Nature 463:E8), Bijma (Bijma et al 2007 Genetics 175:277), Muir (1996 Poultry Science 75:447), Eldakar (Eldakar et al 2010 Evolution 64:3183) Simon (Simon et al 2013 Evolution 67:1561), Ratcliff (2012 PNAS 109:5), Travisano (2004 Trends Microbiol. 12:72), Driscoll (Driscoll and Pepper 2010 Evolution 64:2682) or dare I suggest myself? These are people who understand multilevel selection. I should point out that it is not just this sentence where he fails to cite the relevant literature. With the exception of one vacuous (it will come up later) reference to a paper of mine, none of these authors appear in the literature cited.

This is a fundamental problem that I am seeing. Gardner, not to mention the authors of the letters to nature that we have been fielding, appear to be completely ignoring the MLS literature. I will admit my own failings in this matter. It is not infrequent that I will glance over an abstract and decide it is not important to what I am writing about. However, when writing outside my field (and yes, Gardner is working outside his field) I really do try to ask colleagues if they know of anything I have missed. In this case there is plenty that Gardner missed. As an example, the model he develops in his paper is totally incompatible with the results of Goodnight and Stevens (1997 Am Nat 150:S59). Nobody but Andy knows the real reason ignored the body of MLS literature. Hopefully it won’t happen in the future.

With these weak foundations, Gardener then goes on to list a series of things that he believes to be difficulties. These include:

  • the “precise meaning of group trait” – A group trait is either a trait measured on the group itself, or a composite of measures taken on the group members. Both can be appropriate. Like all studies of selection an understanding of the underlying biology is needed to identify relevant traits. Bottom line: experimentalists need to actually measure these “group” (really contextual) traits. As you might expect, those who measure them know what they are.
  • The “precise meaning of group fitness” – I have to give you that. However, the reason for this is that it is not relevant to the study of MLS. The relevant issue here is measuring selection in the field, and for this the appropriate approach is contextual analysis, which does not use “group fitness” (see Taylor, Wild and Gardner 2007 J. Evol Biol 20:301 for a demonstration that direct fitness, which is the same thing as contextual analysis, is an appropriate metric, Snideness aside, also look at Goodnight 2013 Evolution 67:1539).
  • There is “ambiguity as the focal level in a MLS analysis”. Here he is complaining about the distinction between multlevel selection 1 and 2. I do not like this language, and I am not the best to comment on it. The term was coined over 25 years ago, can we give it a rest? The basic problem is the level at which you assign fitness. Sadly he again shows his ignorance because the actually most relevant paper that gives a relatively simple explanation for this non-controversy is the one paper of mine he cites: Goodnight 2013 (pp 37-53 in: From Groups to Individuals). Sadly, while he did cite this chapter, it was not in the context of this problem, and when he did cite it, it is to make an invalid point.
  • Finally, he makes a big deal about MLS theory does not adequately able to handle class structured populations. First, off, there actually is a nice old paper on multilevel selection in age-structured populations (Mertz et al 1984 Evolution 38:560), although it really isn’t very useful in this context. More relevant, the reason that nobody has developed a method to study MLS in a class-structured population is that nobody has bothered – Most ant people these days are kin selectionists. The basic approach is actually conceptually quite simple:   I would follow Lande’s lead on analyzing sexual dimorphism (Lande 1980 Evolution 34:292) and phenotypic plasticity (Via and Lande 1985 Evolution 39:305). I would describe a separate trait for each cast, plus one or several contextual traits to describe the overall composition of the colony. Each individual would express only one of the individual traits, but of course, all would experience the contextual traits. Then it would be a small matter to modify the methods of Lande and Via and Lande to use them in this system. It actually isn’t that different from the approach Gardner advocates, but it is far more elegant, and it is far more consistent with the existing methodologies for related problems.

So basically what we see in Gardner’s paper (and by extension many of the letters to Nature) is a failure to be aware of and to understand the relevant literature. The problem is not failure to cite the relevant papers per say, rather the problem is that by they do not know the literature and understand the field. As a result the authors end up looking foolish for raising issues that do not exist, and suggesting methodologies that in this case are clumsy, but as we shall see in the next week or two, also methodologies that simply give the wrong answer. I am aware that it is often easy to miss important papers, but to paraphrase the old saying about the law: Ignorance of the literature is no excuse.


We all are guilty of not adequately reading the literature. Nevertheless, it is something to be avoided.  (From



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