Molecular evolution through the joint lens of genomic and population processes.
Towards an improved understanding of molecular evolution: the relative roles of selection, drift, and everything in between
In their perspective article, F Pouyet and KJ Gilbert (2020), propose an interesting overview of all the processes that sculpt patterns of molecular evolution. This well documented article covers most (if not all) important facets of the recurrent debate that has marked the history of molecular evolution: the relative importance of natural selection and neutral processes (i.e. genetic drift). I particularly enjoyed reading this review, that instead of taking a clear position on the debate, catalogs patiently every pieces of information that can help understand how patterns we observed at the genome level, can be understood from a selectionnist point of view, from a neutralist one, and, to quote their title, from "everything in between". The review covers the classical objects of interest in population genetics (genetic drift, selection, demography and structure) but also describes several genomic processes (meiotic drive, linked selection, gene conversion and mutation processes) that obscure the interpretation of these population processes. The interplay between all these processes is very complex (to say the least) and have resulted in many cases in profound confusions while analyzing data. It is always very hard to fully acknowledge our ignorance and we have many times payed the price of model misspecifications. This review has the grand merit to improve our awareness in many directions. Being able to cover so many aspects of a wide topic, while expressing them simply and clearly, connecting concepts and observations from distant fields, is an amazing "tour de force". I believe this article constitutes an excellent up-to-date introduction to the questions and problems at stake in the field of molecular evolution and will certainly also help established researchers by providing them a stimulating overview supported with many relevant references.
 Pouyet F, Gilbert KJ (2020) Towards an improved understanding of molecular evolution: the relative roles of selection, drift, and everything in between. arXiv:1909.11490 [q-bio]. ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. url:https://arxiv.org/abs/1909.11490
Guillaume Achaz (2020) Molecular evolution through the joint lens of genomic and population processes.. Peer Community in Evolutionary Biology, 100103. 10.24072/pci.evolbiol.100103
Revision round #22020-04-29
Decision round #2
The two referees and myself have carefully read the revised version of your manuscript. All the three of us agree and recognize the great improvement of this version, compared to the previous one. The ms really nows conveys a more balanced and precise review of the interactions of the different processes at stake in the patterns of molecular diversity. Although the improvement of this new version is impressive, I believe that there is still some room for extra minor adjustments. Please read carefully the comments of the two reviewers on this new version and provide a point by point response.
I also would like to suggest on top several minor points that the authors may want to consider. These points can help clarifying or illustrating the scientific content of this version.
1) Effective population size - its first occurrence is, I think on p3. Ne is never defined and this lacks, as there are multiple ways to define and/or to understand Ne. I would encourage the authors to define Ne at its first occurrence, or to avoid this term entirely. I suspect that on p3 the authors meant some sort of "neutral" Ne (e.g. harmonic mean of population size), but some people use the term Ne to refer to "level of diversity" (measured through \pi or any other statistics). As (linked) selection will greatly affect the diversity, replacing "diversity" by "Ne" may lead to very confusing arguments. I know this is a long standing debate, getting back to at least Gillespie (and his articles on the meaning of Ne).
2) I am not a big fan of Figure 1 as it is now. Can the author work a bit to clarify it? I suspect that having more than 2 chromosomes/sequences per sample will be helpful.
3) For meiotic drive, may I suggest the reading of: Henikoff S, Ahmad K, Malik HS: The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001, 293:1098-1102.
4) If I am not too confused, there is a major difference between gBGC and selective sweep. In the former, there is no room for hitchhiking, so the neutral surrounding diversity is not affected. It may be worth mentioning it.
5) Finally, there is no Acknowledgments section in your article. Is this on purpose?
Reviewed by anonymous reviewer, 2020-04-07 15:19
Reviewed by Benoit Nabholz, 2020-04-12 15:09
Revision round #12019-11-22
Decision round #1
Two external reviewers and myself have carefully read and then evaluated your manuscript. All the three of us had mixed feelings about the current version of this review. Although, we all believe this is an important and timely topic, the current version may be too short to cover a large and deep topic of molecular evolution.
Although I cannot recommend the ms in its current version, I truly believe that there is the potntential basis for a more satisfying version, with some extra work. Mainly, you will have to face two choices: (1) either elongate significantly the content (I am aware that most journal editors requires to shorten article as much as possible, so that this recommendation may seem weird) and discuss more generally the interference between drift, selection, demography and/or structure (processes mostly acting at the population scale) together with molecular processes (such as BGC or for example meiotic drive). (2) Another possible choice is to refocus your review on a more specific point and to treat it more deeply.
On a personal note, I share your interest on BGC but believe that it belongs to a larger class of molecular processes on which you could include mutations (a topic on which several new observations and theory have been brought recently), meiotic drive, among others.
If you decide to send a revised version of the manuscript to PCI Evol Biol, please address all the points of the two reviewers and rework your article making an explicit choice between both options I have discussed above. I understand this decision may be a frustrating for you, but be assured that none of the reviewers nor myself have a negative opinion toward the general objective of your review. It is actually quite the opposite, we all have a strong interest in these questions.