General Recommendation: Full Accept

Overall Summary and Thoughts:

This paper begins with what is dubbed “Williams’ Rule” which states that group-level adaptations require a process of group-level selection (p. 3).

The paper goes on to argue that this insight from evolutionary biology should be better known and understood by “readers whose primary interest is to accomplish positive change in real-world settings” (p. 3). The paper argues that positive change usually comes from getting people to cooperate with one another toward a common goal (e.g. reducing carbon emissions), and also that some social harms come from lower-level cooperative groups causing disruption (e.g. cartels).

The paper goes on to discuss that in the 1966 book Adaptation and Natural Selection, George Williams not only lays out the conditions for the evolution of group-level adaptations (group-level selection), but also makes a strong empirical claim: Most of the time, higher-level selection will be weak when compared to lower-level selection. That is, despite the fact that group-level selection can, in theory, lead to group-level adaptation, Williams argued that, in the real world, this would seldom happen.

The paper argues that Williams’ theoretical claim has stood the test of time, but the empirical claim has not, especially when considering cultural evolution.

The paper then goes on to present some examples from biology to a general audience and also weighs in some of the more technical aspects of disagreements within biology.

Overall, I really liked this paper. I share the author’s enthusiasm for sharing insights from evolutionary biology, in particular multi-level selection, with a broader audience. I think the paper is well-written overall, both clear and engaging.

I have some comments, mostly minor, which I hope will further improve the manuscript.

Specific Comments:

* On p. 4, the author writes:

> First, however, it is important to introduce multilevel selection theory on its own terms. The key to applying Williams’ Rule is to make a nested series of relative fitness comparisons. Are there fitness differences among genes within single organisms? If so, then unless they are highly orchestrated (such as the adaptive component of the immune system), they are likely to result in disruptive traits such as meiotic drive and cancer (Agren 2021; Aktipis 2020).

I worry that a general reader may not follow without elaboration. Perhaps explain that meotic drivers violate Mendel’s rules and have a biased advantage of making it into the gametes (i.e. lower-level self-interest), which comes at the cost of lower fitness for the organism (i.e. disruption as the author puts it). I think a bit more of the biology here would help someone not already steeped in this literature.

- On p. 4, the author writes:

> Frameshifting upward, are there fitness differences among individuals within single-species social groups? If so, then unless they are highly orchestrated (such as reputational systems that align status with positive contributions to the group), they are likely to result in disruptive traits such as free-riding, deception, and bullying.

As with the previous comment, I wonder if this needs elaboration. In particular, this framing supposes that there is already some higher-level society which has certain goals that are being thwarted or harmed by “disruptive traits such as free-riding, deception, and bullying.” Without some pre-existing, higher-level society, then this is just a case of individuals pursuing their self-interest. We would not, presumably, label the behavior of birds engaged in competition for nest sites as “free-riding” as we have no sense in which there is some higher-level society of birds that is being harmed by this competition or that wishes it were some other way.

My point is that a term like “free-riding” implies that there has already been some degree of selection for higher-level social structures and systems. Otherwise, it’s just “competition”, right?

In the case of humans intentionally engaged in positive change, channeling the behavior of lower-level entities toward cooperation and coordination so as to achieve higher-level organization will often meet resistance in the form of “disruptive traits such as free-riding, deception, and bullying.” But, this implies the pre-existence of some higher-level order.

- On p. 5, the author discusses the game of Monopoly. I really like this example. It’s compelling and clear. However, I am not sure I follow the last bit: “But there is still not context for cooperation between the teams. For that, we would need to organize a tournament at the level of teams-of-teams.” I get the point. However, the game of Monopoly, as it’s designed, doesn’t leave open any space for interaction across Monopoly boards and so I am not sure what it would mean to have “teams-of-teams.” For this to happen, we would need to redefine the game so that there were interaction across boards. I wonder if this should be cut? If not, then perhaps a bit of elaboration so the reader doesn’t get confused? Indeed, when the author moves on to the discussion of chickens, the contrast is between (a) individual selection and (b) group selection. There is no mention of group-of-group selection, as with Monopoly.

- On p. 7, when discussing beavers, the author writes:

> If we want to understand the nature of beaver ecosystems, the first question to ask is “what’s in it for the beavers?” Flooding the habitat makes clear sense as a defense against terrestrial predators. A preference for trees that are not defended by secondary compounds makes clear sense from the standpoint of optimal foraging theory.

The third sentence in this passage about secondary compounds and optimal foraging theory is confusing without more context. Was there something cut from the original manuscript? If not, this section warrants elaboration including (a) that it’s the beavers that prefer certain kinds of trees, (b) defining secondary compounds, and (c) defining and explaining optimal foraging theory. Some of this is done in the next paragraph, but I worry that readers will be confused about this particular sentence in this paragraph.

- On. p 7, the author writes:

> The word “regime” is used to describe a basin of attraction (e.g., Andersen et al., 2009), which aptly invokes what we already know about human political regimes. A political regime has a degree of stability, or else we wouldn’t use the word, but this says nothing about how well the regime functions for the common good. Human regimes can be despotic in addition to enlightened and the same is true for biological regimes.

This is minor, but I worry that the last sentence can be interpreted incorrectly. The author draws an analogy between political and biological “regimes” in that they are labels to describe some period of stability, but do not describe the nature of that stability. However, a narrow reading of the very last sentence might lead a reader to think that biological regimes, like political regimes, can be characterized as “despotic” or “enlightened,” which is not what the author intended.

- On p. 8, the author writes:

> Laboratory experiments similar to the second chicken experiment provide more evidence that selection can take place at the level of single-species groups, multi-species communities and ecosystems (reviewed by Wade 2016).

I worry that the reader may have forgotten the two different chicken experiments at this point in the paper. Perhaps a different way of referring to the experiment? Perhaps labeling the experiments above as “individual selection” and “group selection” or “coop selection.” Here, these labels can be used, rather than “first” and “second”, to reduce potential confusion.

- On p. 10, the author writes:

> Other mechanisms of inheritance, in addition to genetics, include epigenetics (changes in gene expression rather than gene frequency) forms of social learning found in many species, and forms of symbolic thought that are distinctively human (Jablonka and Lamb 2006).

There should be a comma after the parenthetical ending in “frequency”.

- On pp. 10-11, the author discusses the possibility of intragenerational evolution. I don’t see anything in the text of this section that links back to Williams’ Rule or the notion of “group selection” as the author has been discussing. Could this be elaborated?

- On p. 11, the author discusses Elinor Ostrom’s work on the “core design principles” underlying the successful management of common-pool resources. As it’s currently written, there is nothing here that links to Williams’ Rule. While it may be the case that the successful management of common-pool resources requires certain institutional design principles, there’s nothing in this statement that pertains to group selection. I am not sure if the author is arguing that a deep evolutionary history of group selection has endowed us with a psychological capacity that, today, can be harnessed to manage common-pool resources (genetic group selection in the past) or if there is some kind of selection currently going on between, say, communities who are each attempting to manage common pool resources and this process is what creates and maintains social institutions in those communities for the successful management of common pool resources (cultural group selection in the present). Perhaps the author could elaborate the link between Ostrom’s design principles, on the one hand, and Williams’ Rule and group selection, on the other.

- On p. 11, the author writes:

> The worldwide community of people working toward positive change is highly diverse, include formal efforts designated by the word “policy” and informal efforts that individuals and groups engage in all the time.

The word “include” should be “including” I think.

- On p. 12, the author writes:

> As an historical aide, Smith invoked the metaphor…

The word “aide” should be “aside.”

- In the middle of p. 12, the author writes about complex adaptive systems, including a distinction between a complex system that is adaptive as a system (CAS1) and a complex system composed of agents following their respective adaptive strategies (CAS2).

I wonder if it would help to elaborate. I am somewhat familiar with this distinction, but I worry that readers will not be. Perhaps an illustrative example of each type would be sufficient?

- On p. 12, the author writes:

> As I mentioned at the beginning of this article, there is a growing community of change agents who do have a background in evolutionary biology, are aware of Williams’ Rule, and do not need a basic tutorial for themselves (e.g., Henrich 2004; Waring et al. 2015; Brooks et al., 2018; Kline et al., 2018).

I am not really sure what the author means by “change agents” (both here and elsewhere). For example, three of the citations are seemingly geared toward policy and intervention, but the paper by Henrich (2004) is not. That paper was written for an economics journal and was meant to introduce the concept of cultural group selection to business and economics types.

- On pp. 12-13, the author discusses the equivalence between different perspectives on social evolution, including the discussion of “trait groups,” a concept the author introduced in 1975, and calls for unity.

I am fully sympathetic with the author’s point about equivalence among perspectives. However, I worry this call for unity masks disagreements about how various concepts are defined within the field of biology.

For example, at various points in the paper, the author discusses the concepts of “relative fitness” and “group selection” in the context of social evolution. I know what the author means by these terms, but I wonder whether it is worth citing and engaging, if only to acknowledge, that some in biology use these terms in different ways. In particular, what the author calls “group selection” is sometimes broken up into two different concepts: “trait group selection” and another type of group selection, which specifically refers to the problem of altruism (e.g. Nunney 1985 The American Naturalist 2: 212-230).

Likewise, in some circles, the term “altruism” is reserved for behavior that reduces the fitness of the actor in order to provide some fitness increase to other individuals (e.g. West et al. 2007 Journal of Evolutionary Biology 20: 415-432). Many of the behaviors described in this paper would be deemed “weak altruism” or “cooperation” but not “strong altruism” on those definitions. I don’t say this to disagree, but there are different definitions for some of these terms and I wonder if it would help to at least acknowledge some of this variation, perhaps in a footnote.

On p. 13, the author indeed engages with this debate and asks us to “go beyond these assumptions.” I fully agree with this approach and find it useful to talk about the spread of traits among groups in terms of “group selection.” However, I wonder if this section would be made stronger if the author were to spend a bit more time talking about how various terms in this paper (e.g. fitness, group selection) are used differently by different people in biology.

- On p. 15, the author writes:

> Sometimes, higher-level selection takes place all by itself without requiring the assistance of policymakers. For example, some of the common-pool resource groups studied by Elinor Ostrom 1990; see Cox et al. 2010 for an additional sample of groups) had implemented the core design principles without needing to be coached, which is how Ostrom was able to derive them in the first place. The flipside of this coin is that many other common-pool resource groups did not implement the core design principles on their own and therefore were not sustainably managing their resources. Work is required for these groups to become more sustainable, which often involves addressing power imbalances in addition to educative efforts.

I am not well-steeped in this body of research, so I may be wrong here. But it seems to me that the self-organization of a group to the successful management of common-pool resources is not, in and of itself, an example of “higher-level selection.” If it were the case that there were multiple such groups who were competing among themselves such that institutional arrangements that better managed the commons spread when compared to other institutions, that would constitute “higher-level selection.” But it seems to me that a group that finds a way to manage itself is not sufficient evidence. Perhaps the author could elaborate?

- On pp. 15-16, the author writes:

> Some of the insights for positive change efforts that flow from Williams’ Rule include the following (see Wilson et al. 2023 and Wilson and Snower 2024 for a more extensive treatment):

> - The welfare of the whole earth system must be the ultimate unit of selection. Any other target of selection runs the risk of becoming disruptive at higher scales.

I am not sure I completely understand. If we take the whole earth system as a “unit of selection” then what is this unit competing against in some form of higher-level selection? I have seen this kind of statement made in the context of using multi-level selection to address the issue of climate change. Is this the kind of thing the author has in mind? If so, I don’t really see how this works as there is no sense in which our planet is competing with other planets. Perhaps the author can elaborate and clarify?