From populations to subspecies… to species? Contrasting patterns of local adaptation in closely-related taxa and their potential contribution to species divergence
Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST – FST comparisons
Recommendation: posted 14 May 2020, validated 14 May 2020
Porcher, E. (2020) From populations to subspecies… to species? Contrasting patterns of local adaptation in closely-related taxa and their potential contribution to species divergence. Peer Community in Evolutionary Biology, 100097. 10.24072/pci.evolbiol.100097
Elevation gradients are convenient and widely used natural setups to study local adaptation, particularly in these times of rapid climate change [e.g. 1]. Marin and her collaborators  did not follow the mainstream, however. Instead of tackling adaptation to climate change, they used elevation gradients to address another crucial evolutionary question : could adaptation to altitude lead to ecological speciation, i.e. reproductive isolation between populations in spite of gene flow? More specifically, they examined how much local adaptation to environmental variation differed among closely-related, recently diverged subspecies. They studied several populations of two subspecies of snapdragon (Antirrhinum majus), with adjacent geographical distributions. Using common garden experiments and the classical, but still useful, QST-FST comparison, they demonstrate contrasting patterns of local adaptation to altitude between the two subspecies, with several traits under divergent selection in A. majus striatum but none in A. majus pseudomajus. These differences in local adaptation may contribute to species divergence, and open many stimulating questions on the underlying mechanisms, such as the identity of environmental drivers or contribution of reproductive isolation involving flower color polymorphism.
 Anderson, J. T., and Wadgymar, S. M. (2020). Climate change disrupts local adaptation and favours upslope migration. Ecology letters, 23(1), 181-192. doi: 10.1111/ele.13427
 Marin, S., Gibert, A., Archambeau, J., Bonhomme, V., Lascoste, M., and Pujol, B. (2020). Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from QST – FST comparisons. Zenodo, 3628168, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. doi: 10.5281/zenodo.3628168
 Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323(5915), 737-741. doi: 10.1126/science.1160006
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article. The authors declared that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article.
Evaluation round #2
DOI or URL of the preprint: https://doi.org/10.5281/zenodo.3628168
Version of the preprint: 2
Author's Reply, 12 May 2020
Decision by Emmanuelle Porcher, posted 16 Apr 2020
Decision on your preprint "Potential adaptive divergence between subspecies and populations of snapdragon plants inferred from Qst-Fst comparisons"
Dear Sarah Marin,
Thank you for submitting a revised version of your manuscript to PCI Evolutionary Biology, and for answering one critical question so rapidly. This version has been evaluated by two reviewers, whose comments are hopefully attached to this message (if not, let me know). First, I would like to renew my apologies for the extremely long time it took me to return this decision. This is due to the pandemics, but still, this excuse is of no great comfort to you. As you will see, both reviewers found that the new, and significantly modified, version of your article is greatly improved. The question of the calculation of Qst is now solved, and I agree that it does not modify the main results of your study, such that I will be happy to recommend it for PCI Evolutionary Biology provided you make the few relatively minor changes suggested by both reviewers and myself.
Thank you very much for submitting your preprint for recommendation in PCI Evolutionary Biology.
Abstract: the words « potential » or « potentially » appear 6 times in the abstract. It is good to be cautious but surely some of these could be reworded (check lines 21-24 out in particular)
Line 249: I am not sure what “linearized” means here
Line 263: replace ‘last’ with ‘latter’
Lines 282-285: this latter analysis seems to be the most comprehensive, and the one you really need to address your main questions. What is the point of the other Mantel tests described above?
Lines 312-317: Could you confirm that the difference in the correlation between trait values and altitude between the two taxa is not due differences in the variance in altitude across populations for each taxon? Is variance in altitude the same for both taxa?
Lines 332-336: do you mean that the results obtained via the examination of overlapping confidence intervals are fully consistent with those obtained by the bootstrapping method? If so, this is not entirely clear from this sentence.
Lines 384 and 385: replace two instances of “less” with “fewer”
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Reviewed by Santiago C. Gonzalez-Martinez, 10 Apr 2020
Reviewed by anonymous reviewer 1, 09 Apr 2020
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/385377
Author's Reply, 27 Jan 2020
Decision by Emmanuelle Porcher, posted 16 Oct 2018
Dear Sara Marin,
I would first like to apologize for the time needed to return this decision, which is partly attributable to the difficulty of finding available reviewers in the middle of summer. Your preprint has now been read carefully by two experts (including Sophie Karrenberg (SK), who signed her review) and by me. We all agree that your manuscript addresses and important evolutionary question (patterns of adaptation to altitude), and that the experimental design was appropriate to address this question, such that I would ultimately be willing to recommend this preprint provided you can address the issues raised by the reviewers. Here are the most critical issues I identified, some of which were raised independently by both reviewers:
(1) Definition of local adaptation: both reviewers and I were lost with, or at the minimum confused by, your distinction between local adaptation (the meaning of which seems to vary throughout the paper, see comments by SK) and adaptation to latitudinal gradients, which involves local adaptation in the broad sense, such that individuals with the highest fitness in one location are on average those originating from this location. It is really important that this point is clarified. This may include for example specifying whether you consider local adaptation as a pattern or as a process or both. Another option for clarification would be to follow the first suggestion of SK, which is to focus more on biology and the question of adaptation to altitude, and how to disentangle it from adaptation to other environmental variables, which may vary in space at a finer grain than altitude (or not, see comment 7 by reviewer #2)
(2) SK is worried that pooling the two subspecies might bias your analyses. There again, it is central to provide a solid justification for this pooling
(3) Methodological / statistical issues: both reviewers had several additional questions and suggestions regarding the statistical analyses, which I will not fully list here (although they all deserve attention), but which include for example: (i) How could you estimate the within population additive genetic variance, when the number of individuals and the number of families seem to be similar (i.e. about one individual per family)? (ii) How was the significance of the relationship between Fst (or Qst) and altitudinal differences tested in Figure 3? (iii) On the same figure, can the statistical significance of the differences in slopes be tested? More generally, the two reviewers often requested more details on the methodology (e.g. Qst-Fst comparisons, quantitative genetics analyses…), and I agree with them that some key information is sometimes missing.
(4) While the “Methods” section could be expanded, the two reviewers and I agreed that the text could also be shortened at places, particularly in the discussion.
Thank you very much for submitting your preprint for recommendation in PCI Evolutionary Biology. I hope you will find this feedback, and particularly the very thorough reviews of the experts, useful to revise your manuscript.
Best regards Emmanuelle