Recent assembly of European biogeographic species pool
Pleistocene climate change and the formation of regional species pools
Biodiversity is unevenly distributed over time, space and the tree of life . The fact that regions are richer than others as exemplified by the latitudinal diversity gradient has fascinated biologists as early as the first explorers travelled around the world . Provincialism was one of the first general features of land biotic distributions noted by famous nineteenth century biologists like the phytogeographers J.D. Hooker and A. de Candolle, and the zoogeographers P.L. Sclater and A.R. Wallace . When these explorers travelled among different places, they were struck by the differences in their biotas (e.g. ). The limited distributions of distinctive endemic forms suggested a history of local origin and constrained dispersal. Much biogeographic research has been devoted to identifying areas where groups of organisms originated and began their initial diversification . Complementary efforts found evidence of both historical barriers that blocked the exchange of organisms between adjacent regions and historical corridors that allowed dispersal between currently isolated regions. The result has been a division of the Earth into a hierarchy of regions reflecting patterns of faunal and floral similarities (e.g. regions, subregions, provinces). Therefore a first ensuing question is: “how regional species pools have been assembled through time and space?”, which can be followed by a second question: “what are the ecological and evolutionary processes leading to differences in species richness among species pools?”.
To address these questions, the study of Calatayud et al.  developed and performed an interesting approach relying on phylogenetic data to identify regional and sub-regional pools of European beetles (using the iconic ground beetle genus Carabus). Specifically, they analysed the processes responsible for the assembly of species pools, by comparing the effects of dispersal barriers, niche similarities and phylogenetic history. They found that Europe could be divided in seven modules that group zoogeographically distinct regions with their associated faunas, and identified a transition zone matching the limit of the ice sheets at Last Glacial Maximum (19k years ago). Deviance of species co-occurrences across regions, across sub-regions and within each region was significantly explained, primarily by environmental niche similarity, and secondarily by spatial connectivity, except for northern regions. Interestingly, southern species pools are mostly separated by dispersal barriers, whereas northern species pools are mainly sorted by their environmental niches. Another important finding of Calatayud et al.  is that most phylogenetic structuration occurred during the Pleistocene, and they show how extreme recent historical events (Quaternary glaciations) can profoundly modify the composition and structure of geographic species pools, as opposed to studies showing the role of deep-time evolutionary processes.
The study of biogeographic assembly of species pools using phylogenies has never been more exciting and promising than today. Catalayud et al.  brings a nice study on the importance of Pleistocene glaciations along with geographical barriers and niche-based processes in structuring the regional faunas of European beetles. The successful development of powerful analytical tools in recent years, in conjunction with the rapid and massive increase in the availability of biological data (including molecular phylogenies, fossils, georeferrenced occurrences and ecological traits), will allow us to disentangle complex evolutionary histories. Although we still face important limitations in data availability and methodological shortcomings, the last decade has witnessed an improvement of our understanding of how historical and biotic triggers are intertwined on shaping the Earth’s stupendous biological diversity. I hope that the Catalayud et al.’s approach (and analytical framework) will help movement in that direction, and that it will provide interesting perspectives for future investigations of other regions. Applied to a European beetle radiation, they were able to tease apart the relative contributions of biotic (niche-based processes) versus abiotic (geographic barriers and climate change) factors.
 Rosenzweig ML. 1995. Species diversity in space and time. Cambridge: Cambridge University Press.
 Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters. 10: 315–331. doi: 10.1111/j.1461-0248.2007.01020.x
 Lomolino MV, Riddle BR, Whittaker RJ and Brown JH. 2010. Biogeography, 4th edn. Sinauer Associates, Inc., Sunderland, MA.
 Wallace AR. 1876. The geographical distribution of animals: with a study of the relations of living and extinct faunas as elucidating the past changes of the earth's surface. New York: Harper and Brothers, Publishers.
 Calatayud J, Rodríguez MÁ, Molina-Venegas R, Leo M, Hórreo JL and Hortal J. 2018. Pleistocene climate change and the formation of regional species pools. bioRxiv 149617 ver. 4 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/149617
Fabien Condamine (2018) Recent assembly of European biogeographic species pool. Peer Community in Evolutionary Biology, 100053. 10.24072/pci.evolbiol.100053
Revision round #212 May 2018
Decision round #2
Thank you again for soliciting the Peer Community in Evolutionary Biology to evaluate your study.
I have now received the feedback of one of the three reviewers for your preprint study (see below). You will see that the referee is very positive about the revision. In addition, the referee identified little mistakes/typos that should be corrected to improve the study. Overall, I agree with the reviewer that the study is both solid and interesting. As I said, I think the approach is thorough and original, which may be useful for further studies looking at effect of glaciation effects on regional species pools. The study is now strong on the methodological aspects like phylogenetic and dating analyses.
To summarize, the authors have addressed the major (6) points raised by the reviewers including: (1) The re-writing and re-structuring of the paper. This is now much clearer. (2) The hypotheses tested are better presented, and it’s clear. (3) The phylogenetic and dating analyses have been re-performed based on the referee’s comments. I really like the presentation of both calibration scenarios. (4) The downstream analyses have been redone with the newly generated time-calibrated phylogeny (comparing the Andujar et al.’s hypothesis and Deuve et al.’s one). (5) The results and discussion take into account the new phylogenetic/dating analyses including the uncertainty of your species placement with the grafting. (6) The results are now better put in the context of existing literature regarding Pleistocene climatic oscillations.
However, I have a last comment regarding the biogeographic analyses. The authors have used the now traditional and popular BioGeoBEARS approach to infer the ancestral states. I am not convinced by the use of the J parameter in DEC models and relatives. This parameter is a microevolutionary process and is not adapted for macroevolutionary inferences: if you think about founder-speciation event then it is more a population genetic event than a real macroevolutionary process. So how are we supposed to estimate such event at a macroevolutionary time-scale? To support my point of view, there is a paper showing that “DEC+J is a poor model of founder- event speciation, and statistical comparisons of its likelihood with DEC are inappropriate” (Ree & Sanmartín 2018, full reference below). This also applies to the DIVA-like and BayArea-like models. For simple inference of ancestral ranges on a fixed phylogeny, a DEC-based model may be defensible if statistical model selection is not used to justify the choice. So in other words, it means that DEC+J cannot be compared to DEC anymore. To have more clues about that, please look at the Ree’s talk at an Evolution meeting: https://www.youtube.com/watch?v=8Cf4hfZI3VY&ab_channel=EvolutionVideos Ref: Ree R.H. & Sanmartin I. (2018) Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. J. Boigeogr., 45, 741-749. https://doi.org/10.1111/jbi.13173
So in summary, I would advise the authors to select one model (DEC or DIVA-like or BayArea-like) and stick to it. My preference will go to the classical DEC model as there are studies showing that it is a very robust model even under complex scenarios (Beeravolu & Condamine 2018, full reference below). I would suggest removing the model comparison that is now flawed. Ref: Beeravolu C.R. & Condamine F.L. (2018) An Extended Maximum Likelihood Inference of Geographic Range Evolution by Dispersal, Local Extinction and Cladogenesis. bioRxiv, https://doi.org/10.1101/038695
Last point, I would strongly suggest the authors to discuss in more details the results of the biogeographic inferences as suggested previously by the referee #1. I think it would bring interesting facts to the paper and for the discussion. It is currently lacking.
Based on the referees’ comments and my last comments, I believe the manuscript will benefit from a slight revision but not followed by a third round of reviews. I hope you are not too disappointed and that you will resubmit a revised paper. For the moment, I do not recommend the study in PCi Evol. Biol. but if the biogeographic results are better explained, I will recommend the paper in PCi Evol. Biol.
Dr. Fabien Condamine, recommender for PCi Evol. Biol.
Reviewed by anonymous reviewer, 21 Feb 2018 18:43
Revision round #113 Feb 2018
Decision round #1
Thank you for soliciting the Peer Community in Evolutionary Biology to assess your study.
We have now received the feedback of three reviewers for your preprint study (see below). You will see that the three referees bring up very interesting and useful comments as well as suggestions that I am sure will improve the study. Overall, I agree with the reviewers that the study has many merits and that the findings are interesting. I also think the approach proposed here is original and may be useful for further studies. However, the study suffers from some methodological issues. I think the main issues concern the phylogeny and dating analyses, but because these results are the cornerstone of the other analyses, the corresponding results may be inconclusive as it stands. The referees also felt that the manuscript suffers from a lack of clarity in several parts of the text. The manuscript would certainly benefit from a careful reading by a native English speaker.
To summarize, I have identified six major points raised by the reviewers that you would need to carefully address. This includes the following: (1) The writing and structure of the paper (in many places the referees have suggested to rephrase the sentence, clarify the meaning, or be more accurate); (2) Clarification of the hypotheses tested (this is an important part of the paper and it needs support from previous studies and the biology of the group); (3) Revising the phylogenetic and dating analyses based on the comments (e.g. using RAxML / MrBayes for the phylogeny and BEAST for the dating with a fixed topology if necessary); (4) Redoing the downstream analyses depending on the newly generated time-calibrated phylogeny (would be great to compare your results with the newly generated tree, and the results obtained with the Deuve et al.’s tree as suggested); (5) Revising the results and discussion based on that new analyses if any change has to be done and including the uncertainty of your results (confidence intervals or credibility intervals); (6) Emphasizing your results in the context of existing literature regarding Pleistocene climatic oscillations and associated effect on biodiversity.
Based on the referees’ comments and my reading, I believe the manuscript will benefit from a revision and a second round of reviews. If you chose to resubmit a revised paper, please make a point-by-point reply to the comments (like for a traditional journal). For the moment, I do not recommend the study in PCi Evol. Biol. but if the revision is thorough (satisfies the reviewers) and the results still support the conclusions, I will be supportive for the paper as being recommended.
Dr. Fabien Condamine, recommender for PCi Evol. Biol.