General Recommendation: Full Accept

Overall Summary and Thoughts:

In this paper, the author discusses how George Williams's argument that adaptation at a given level requires selection at that level can be used to achieve positive societal change. The paper is well written and on a for the author familiar theme. (Indeed, the author has previously discussed the William's insight, but then called it Williams' principle, which I think is a better name.) A couple of comments below that the author may consider, all which largely reflect my own personal preference for and familiarity with inclusive fitness-style explanations.

Page 2, second paragraph.

The author writes "After Darwin, many biologists continued to assume that nature is adaptively organized above the level of the individual organism, such as single-species social groups, entire species, and multi-species ecosystems. The fact that special conditions are required for higher-level adaptations to evolve was not widely appreciated until George C. Williams wrote his book Adaptation and Natural Selection in 1966". I find this bit a little confusing and it seems like second sentence contradicts the first. Wynne Edwards is not cut a lot of slack, but Animal Dispersion was published in 1962 and did recognize that higher-level adaptations required higher-level selection.  

Page 2, bottom

When discussing selection and adaptation at different levels, I think it is important to note that cancers cannot evolve complex adaptations due to the difference in timespan (see discussion by e.g., Howe et al 2022).

Page 3, top

Related to the multilevel version of Williams' Rule. This is similar to what Andy Gardner called Maynard Smith's Principle (to complement Williams'): in order for an entity to evolve adaptations, selection within such entities must be absent or negligible (Gardner 2013, 2014).

Page 4, second paragraph

Two points about the statement "Ongoing debates at the expert level are centered largely on the equivalence and relative merits of alternative accounting methods, as described in more detail below.":

1. This might be minor nitpicking, but inclusive fitness proponents would argue that inclusive fitness is not just another accounting method. It, and only it, is the answer to the design question of what organisms should appear designed to maximize (e.g., West and Gardner 2013)

2. It is true that the debate is partly about accounting methods, but I think one of the most important recent papers on the topic is Birch's 2019 one, which makes the case that we should critically evaluate what 'equivalence' actually means and worry more about how models may be mathematically equivalent they may be causally non-equivalent.  

Page 4, bottom

Re. Frame shifting up and down. I think we need to be careful to compare like with like. Selection at the individual level is measured in terms of new offspring individuals, whereas the kind of group selection that is invoked is the MLS1 kind that does not measure fitness in terms of new daughter groups, but number of individuals contributed to overall pool. Is it worth introducing the MLS1 vs MLS2 distinction here? Or too much?

Page 9, last paragraph

Another relevant paper here is Patten et al's one on the paradox of the organism (2023).

Page 10, mid

"Continuing the tutorial part of this article...." This part felt less like a tutorial and more like a telling. Each point is very brief and therefore not given enough time to be explained. For example, on Page 11, top, the author writes "The open-ended capacity for behavioral change based on a history of reinforcement, which B.F. Skinner (1981) called “selection by consequences”, can also be regarded as an intragenerational evolutionary process." This comes seemingly out of nowhere. I think Skinner needs to be introduced more thoroughly or dropped. I found the section on kind and mean humans equally frustrating for this reason (page 11).

Page 10, fourth paragraph

The author writes "Our species is part of the elite club that has undergone a MET, from groups of organisms to groups as organisms (Szathmary 2015; Wilson et al. 2008)." This statement surprised me, and the use seems to be out of step with how the term is usually used, I therefore tried to find how the author defines a major transition, as it seems to be out step with out how it is currently used. In "Generalizing the core design principles for the efficacy of groups", Wilson et al write: "All of the hallmarks are present: It was a rare event, occurring only once among primates. It had momentous consequences once it occurred; we are the dominant species on the planet, for better or for worse. It is far from complete; within-group selection still operates and anti-social behaviors are suppressed to the degree that they are only by virtue of an arsenal of social control mechanisms that keep them under control." This definition is rather quite different from how it is used by people like Andrew Bourke (2011) and Koos Boomsma who have written recent books on the topic, use it. Similarly, in a major review West et al. define major transitions in general, and transitions in individuality in particular, as:

"A major evolutionary transition has been most broadly defined as a change in the way that heritable information is stored and transmitted. We focus on the major transitions that lead to a new form of individual (Table 1), where the same problems arise, in a way that facilitates comparison, and so exclude the evolution of the genetic code, sex and language. A major evolutionary transition in individuality is defined by two conditions. First, entities that were capable of independent replication before the transition can replicate only as part of a larger unit after it, termed mutual dependence, interdependence, or contingent irreversibility. Second, there is a relative lack of within-group conflict such that the larger unit can be thought of as a fitness- maximizing individual (or organism) in its own right". West et al explicitly reject humans as a major transition for this reason.

Page 12, top

"the first native American tribes to gain access to guns and to master horseback riding used their power advantage against other native American tribes (Gwynne 2011; Silverman 2016)." I don't follow this point. Similarly, the discussion about CAS1 vs CAS2 is too brief to be helpful for someone not already familiar. (This might contradict my wish above to introduce the MLS1 vs MLS2 distinction and may reflect my own background.)

Page 12, bottom

"Yet, major thinkers such as Dawkins (1994) and Pinker (2012) still treat different theoretical frameworks as if they invoke different causal mechanisms, such that one can be rejected in favor of the other" Is the Dawkins reference really fair? My impression is that the equivalence consensus came after that (Hamilton 1975 non-withstanding).

Page 13, first paragraph

"Something more is required to explain the evolution of such a prosocial behavior and that “something” is the existence of many such groups, variation in the frequency of the prosocial behavior among the groups, and the differential contribution of the groups to total evolving population" Here is an example where the MLS1 vs MLS2 distinction would be helpful, as it highlights the difference that while major transitions in individual framework (as in the West et al. definition above) shows how you can think of multicellular organisms as group selection at the cellular level, that kind of group selection is different than the, also valid, trait-group selection models.

Page 14, bottom

"This reasoning is based on the early simplifying assumptions outlined above and does not reflect more recent thinking based on complex interactions." Clarify that how much heritability there is in microbiomes is ultimately an empirical question?  

Pages 15-16: "Using Williams’ Rule to Inform Positive Change Efforts"

I was a little underwhelmed by how short this section was. While the paper does a good job of introducing the concept of Williams's Rule and the models and data underlying it, the paper is actually very light on how it can inform policy decisions. For example, "The welfare of the whole earth system must be the ultimate unit of selection" (page 16) sounds very Gaia-ish, but I genuinely cannot tell if that is what is meant. Needless to stay selection in a population of size 1 (one earth) is very different than any scenario discussed previously, as Gaia converts like Ford Doolittle would be the first to concede. I'm also not a huge fan of the point that human groups are like cells, despite its long tradition, and if anything I think it needs to be clear whether it is in the fashion of Herbert Spencer, Rudolf Steiner, or someone else that is intended.  

Finally, thanks again for sending this essay to me. I enjoyed reading it even if I don't agree with all points.


Birch, J. (2019). Are kin and group selection rivals or friends?. Current Biology, 29(11), R433-R438.

Boomsma, J.J., 2022. Domains and major transitions of social evolution. Oxford University Press.

Bourke AFG. 2011. Principles of Social Evolution. Oxford University Press.

Gardner A (2013) Adaptation of individuals and groups. In: From groups to individuals (F Bouchard & P Huneman, eds), MIT Press.

Gardner A (2014) Genomic imprinting and the units of adaptation. Heredity 113, 104-111.

Howe, Jack, et al. 2022. "Multicellularity in animals: The potential for within-organism conflict." Proceedings of the National Academy of Sciences 119.32: e2120457119.

Patten, M. M., Schenkel, M. A., & Ågren, J. A. (2023). Adaptation in the face of internal conflict: the paradox of the organism revisited. Biological Reviews.

West SA & Gardner A (2013) Adaptation and inclusive fitness. Current Biology 23, R577-R584.

West, S.A., Fisher, R.M., Gardner, A. & Kiers, E.T. (2015) Major evolutionary transitions in individuality. Proceedings of the National Academy of