Ecological diversification in rapidly evolving populations

Reviewer #1 (Public review):

Summary:

This important study performs a theoretical analysis of the evolutionary dynamics of strains under a classical resource competition model to understand how clonal interference and diversification of resource preferences interact to structure microbial population genetic structure. They find that in large asexual populations evolving in relevant parameter regimes, where evolutionary and ecological time scales overlap, populations are characterized by a small number of ecotypes, which are groups of strains that share a given resource preference, whose dynamics in the long run are dominated by priority effects.

Strengths:

The manuscript constitutes a novel and sound contribution to theory in ecology and evolution, under relevant parameter regimes which have been previously overlooked due to the complexities they bring, i.e. when the weak mutation regime breaks down. Here, the authors make a considerable step forward by taking advantage of analytical advances in the population genetics theory of clonal interference in recent years (travel fitness wave moving at a constant average speed v), which they apply to resource competition models typically studied in ecology.

The main insights in the derivations shown in the supplementary text are clearly summarized in Figure 2 of the main manuscript, where the different phases of the somewhat counterintuitive dynamics of the strategic mutations in the model are quantified.

Weaknesses:

Despite its many merits, I believe the manuscript can profit from a few clarifications as I point out below:

(1) I think the authors should make explicit in the abstract of the paper that they study a stair to heaven fitness landscape and that the rate of beneficial mutations does not slow down.

(2) Evolution is elegantly incorporated in the resource consumption model by assuming two classes of mutations: strategic mutations and constitutively beneficial mutations. I believe that the biological meaning of these different types should be better explained. Specifically, on pages 3 and 4, the authors state that strategy mutations "alter resource uptake strategy and potentially its overall magnitude as well", whereas the other type is "only tangentially related to resource consumption (e.g. eliminating a pathway that is not necessary in the current environment)." I find this a bit strange since this is a model of resource competition, and I would assume that the latter type of mutations would be neutral. Maybe I am not reading this well, and the meaning of the mutations, as well as their assumed rates, could be clarified with some examples as the authors state that these mutations are routinely observed in microbial evolution experiments.

(3) The authors discuss the theoretical results obtained in the light of the famous Lenski experiment, where ecotype formation is observed in some populations. However, in the mentioned example, cross-feeding was the mechanism involved. Since in their model, unlike in other models, cross-feeding is not considered, I found this example to be misplaced. In addition, in the Lenski experiment, a single (and essential) resource is present in the environment, so the assumptions of the model do not appear to apply. On the other hand, in Herron and Doebeli's experiments, two resources (substitutable) were present, so a comparison with their experimental results would be more appropriate.

(4) The paper should also discuss deleterious mutations, which I did not see mentioned anywhere.

Reviewer #2 (Public review):

Summary:

In "Ecological diversification in rapidly evolving populations", the authors use a consumer-resource model with competition for 2 different resources to study diversification for cases in which ecology and evolution are separated (weak-mutation limit) and when they overlap. They find the potential for the timing of a mutation (and not just its associated fitness) to confer an advantage against fitter strains (which they call "priority effect"), and the aggregation of dominant trait values that lead to the definition of "ecotypes" that discretize and structure the community.

Strengths:

The authors introduce detailed analytical calculations in the limit of overlapping ecology and evolution, which is a case that typically eludes analysis. The work also pays particular attention to the timing of "invasion" by a mutation, whereas most approaches focus on the long-term outcome of evolution (e.g. fixation of a trait value).

Weaknesses:

The model makes important assumptions that limit its generality considerably. In particular, the two "evolving traits" defined in the model are very specific and by no means the simplest possible resource competition evolutionary model that the authors claim it to be. The manuscript is not clear enough to be reproducible, and the authors do not discuss in sufficient depth the huge amount of work that is presented in the manuscript. The bibliography omits important work focused on diversification emerging from eco-evolutionary interactions similar to the ones studied in the manuscript.

Author response:

We thank the Editor and the Reviewers for their detailed and constructive feedback. We look forward to submitting a revised version of the manuscript that addresses their comments and suggestions, with a special focus on clarifying the assumptions and implications of our analysis. In particular, we will aim to demonstrate that (i) many of our qualitative findings -- and even some quantitative results -- extend beyond the simplest two-resource case considered in the main text, and (ii) that they can also be generalized to account for simple forms of cross-feeding. We hope that these changes will help to illustrate the broader applicability of our underlying mathematical framework.