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Summary

  • The initial submission of this article was received on June 16th, 2021 and was peer-reviewed by 2 reviewers and the Academic Editor.
  • The Academic Editor made their initial decision on July 16th, 2021.
  • The first revision was submitted on November 9th, 2021 and was reviewed by 1 reviewer and the Academic Editor.
  • A further revision was submitted on February 8th, 2022 and was reviewed by 1 reviewer and the Academic Editor.
  • A further revision was submitted on March 14th, 2022 and was reviewed by 1 reviewer and the Academic Editor.
  • The article was Accepted by the Academic Editor on April 6th, 2022.

Version 0.4 (accepted)

· Apr 6, 2022 · Academic Editor

Accept

Reviewer 2 raised some minor issues that needed to addressed. Please check the manuscript carefully. I have no other comments.

[# PeerJ Staff Note - this decision was reviewed and approved by Julin Maloof, a PeerJ Section Editor covering this Section #]

[# PeerJ Staff Note: Although the Academic and Section Editors are happy to accept your article as being scientifically sound, a final check of the manuscript shows that it would benefit from further editing. Therefore, please identify necessary edits and address these while in proof stage. #]

Reviewer 2 ·

Basic reporting

No coments

Experimental design

No comentsNo coments

Validity of the findings

No coments

Additional comments

The authors responded satisfactorily to all my comments. I suggest that it should be published as it is (note that some minor corrections are listed below).

Line 84. Duplicated comma
Line 133. The R package is mentioned using quotation marks ' ', however, in subsequent paragraphs the quotations marks are not used (for example l. 144,145), please use the same format.
Line 150. Change the capital letter in "Based"
Line 341-342. Change the capital letters on "Land use/Cover"

Version 0.3

· Mar 10, 2022 · Academic Editor

Minor Revisions

Although the previous comments have been fully addressed, there are some issues that need further consideration.

Reviewer 2 ·

Basic reporting

The authors addressed all the previous comments. Also, this version shows a notable improvement; however, there are some details that should be addressed. For example, spaces between words and parenthesis are frequently missed. Please see the suggestions for details.

Experimental design

No comment

Validity of the findings

No comment

Additional comments

Line 45. There is an incomplete reference, and the phrase should start with a capital letter.
Line 55. Consider changing "There is now" to "Currently, there is"
Line 66. Remove "of" and replace it for a coma.
Line 67. Add spaces before parenthesis in "forests(Zhang" and "slopes(Zhang"
Line 87. Add a space after "sorting;"
Line 106. Change "Individual plants sampled grew at" for "Individual plants were sampled at"
Line 121. There is a mistake in "Ma(Ma et al"
Line 124. The reference of PHASE software is missing in the text and in the References section. Please rephrase this sentence; it is not clear.
Lines 134-137. Were both programs used to estimate GST and NST? I believe that one was for the estimation and the other for the significance; please clarify.
Line 162. Change "Fig Tree" for "FigTree" and add the reference.
Line 164. Add a space before the parenthesis.
Line 178. Consider to change the phrase for "A non-significant value (p>0.05) of SSD and Hraf indicated .... "
Line 238. Add a space in "Clade1"
Line 268. The word "range" is split.
Lines 284, 291, 295, 296. The study species is misspelled.
Line 294. Use capital letters for "Miroc". Also, specify in Methods that this model was used.
Line 299. Add a space in "overallgenetic".
Line 302. Use capital letters for "Maxent".
Line 341-342. This phrase is not clear. Please rewirite.
Line 379. Use "warmer".
Line 388. Consider replacing with "...accompanied by low genetic variation, could...".
Line 397. Move "however" to the beginning.
Figure caption 6. There is an incomplete phrase in "the grouping of populations consistent".

Version 0.2

· Jan 6, 2022 · Academic Editor

Minor Revisions

Generally, this manuscript has been well revised. However, as the reviewer mentioned there are still some points that need improvement, especially the English. Please carefully consider the reviewer comments.

Reviewer 2 ·

Basic reporting

In general, the manuscript is understandable; however, the English still needs some polishing. See comments for examples.

Experimental design

No comment.

Validity of the findings

No comment.

Additional comments

The present version of the manuscript shows notable improvement, and most of the comments were properly assessed. However, there are some points about the demographic analyses that still need clarifying.

Line 289:
"But postglacial range expansion had been demonstrated for the overall populations and two groups by the unimodal mismatch distribution"
I'm not sure if the range expansion is demonstrated. Please, tune down this kind of categorical statement, use "indicated" or "suggested."

In line 293, the authors state:
"However, only the Bayesian skyline plot (BSP) result of overall populations of nDNA was consistent with species expansion."

These results should be presented and interpreted as they are: the three tests for the cDNA displayed an effective size contraction, while the nDNA showed a slight size change by group, and the overall analysis displayed a contraction followed by small population growth.
At this point, it is needed to consider: What is the demographic signal expected in the glacial scenario? If my interpretation is correct, there should be a population contraction caused by the non-favorable conditions followed by a recent range expansion; however, only the contraction signal may be recovered if the expansion is very recent. Thus, the BSP results are somewhat in agreement with the authors' premise. Nevertheless, there are some questions left: Why are discrepancies between the markers? Maybe these are the consequence of differences in the markers' intrinsic effective size (haploid plastid vs. nuclear) and/or in mutation rate? Consider these points to be addressed in the Discussion.

Some specific comments:

Please, in Figure 1, include a mini-map showing the location of the area of study on a broader scale.

The legend of Figure 4 has a duplicated sentence.

Line 45. Consider splitting the sentence "plant growth. For example,".
Line 74. remove "the" in "...2015), the altitude more than ...".
Line 75. remove the comma in "..Plateau), ".
Line 76. Remove "And" and "which".
Line 77. Add "by" "..in valleys, and by the Helan..".
Line 105. Consider rephrasing as "..sites are the same as our team's previous study..".
Line 106. Replace "including 3" with "including three". Remove "..are presented in Table 1." an just use "(Table 1)".
Line 137. Correct the format of the parenthesis in "(GST, NST)".
Line 138. Remove "using Permut 2.0".
Lines 106,105,165,218,219,232. Check the spaces before and after parenthesis.
Line 172. Replace "burn in" for "burnin" or "burn-in".
Lines 174-183. Maybe you should state at the beginning of the sentence that all these tests were implemented with Arlequin.
Line 293. Add "the" before "Bayesian".

Version 0.1 (original submission)

· Jul 16, 2021 · Academic Editor

Major Revisions

I have received comments from two reviewers. Both reviewers found the manuscript interesting, but they also raised some major concerns. For example, Reviewer 1 pointed out that the manuscript lacks more robust analyses to support some statements. Reviewer 2 mentioned that some sections, especially the results need a more detailed explanation. Also, both reviewers made some specific comments that I do think will help the authors improve the manuscript going forward.

[# PeerJ Staff Note: Please ensure that all review and editorial comments are addressed in a response letter and any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate.  It is a common mistake to address reviewer questions in the response letter but not in the revised manuscript. If a reviewer raised a question then your readers will probably have the same question so you should ensure that the manuscript can stand alone without the response letter.  Directions on how to prepare a response letter can be found at: https://peerj.com/benefits/academic-rebuttal-letters/ #]

[# PeerJ Staff Note: The review process has identified that the English language must be improved. PeerJ can provide language editing services - please contact us at copyediting@peerj.com for pricing (be sure to provide your manuscript number and title) #]

Reviewer 1 ·

Basic reporting

The English language should be improved to ensure that an international audience can clearly understand the text. Here some examples where the language could be improved:
L16 – that is occurred | that occurs
L29 – have experienced | to have experienced
L46 – mosaic fragment | fragmented mosaics? Mosaic fragmented landscapes?
L61 - ... occurs from | … that occurs from …
L64 – concentrate | concentrates or is concentrated

Experimental design

, I found their manuscript lacks more robust analyses to support some statements. Thus, to better support their results about the restricted gene flow between western and eastern groups I would recommend the implementation of demographic analyses that explicitly test it. Several approaches could be used to draw demographic models. For instance, an approximated likelihood framework could be used to evaluate thousands of distinct models. A relatively recent tool is PHRAPL (https://phrapl.github.io/). Here are two papers that used it to infer demographic models:
Oliveira et al. 2018. Phylogeography of Muller's termite frog suggests the vicariant role of the Central Brazilian Plateau. Journal of Biogeography. 10.1111/jbi.13427
Everson et al. 2020. Speciation and gene flow in two sympatric small mammals from Madagascar, Microgale fotsifotsy and M. soricoides (Mammalia: Tenrecidae). Molecular Ecology. 10.1111/mec.15433
A second alternative is implementing an Approximate Bayesian Computation (ABC) approach. DIYABC (http://www1.montpellier.inra.fr/CBGP/diyabc/) and PipeMaster (https://github.com/gehara/PipeMaster) are just two tools off the top of my head that are relatively easy to understand and to be used, with good tutorials available. Here are two papers that used them:
Garg et al. 2020. Last Glacial Maximum led to community-wide population expansion in a montane songbird radiation in highland Papua New Guinea. BMC Evolutionary Biology. 10.1186/s12862-020-01646-z
Thom et al. 2020. Climatic dynamics and topography control genetic variation in Atlantic Forest montane birds. Molecular Phylogenetics and Evolution. 10.1016/j.ympev.2020.106812
And, of course, the authors could implement their own ABC approach using the ‘abc’ package, from R (the vignette: https://cran.r-project.org/web/packages/abc/vignettes/abcvignette.pdf)
Another exciting path in model-based phylogeography is machine learning, although I am not sure if so few loci are right for this kind of analyses. The authors could be inspired by these papers:
Flagel et al. 2019. The unreasonable effectiveness of convolutional neural networks in population genetic inference. Molecular Biology and Evolution. 10.1093/molbev/msy224
da Fonseca. 2020. Phylogeographic model selection using convolutional neural networks. Molecular Ecology Resources. 10.1111/1755-0998.13427
The author also discuss that the environmental heterogeneity promotes differentiation between the two groups. The authors should also implement some analyses to support this statement. I recommend the generalized linear mixed modelling (GLMM) approach to test whether population genetic structure is driven by the environment or other variables. Refer to these papers for some examples:
Dantas-Queiroz et al., 2021. Underlying microevolutionary processes parallel macroevolutionary patterns in ancient neotropical mountains. Journal of Biogeography. 10.1111/jbi.14154
Lexer et al., 2014. Genomics of the divergence continuum in an African plant biodiversity hotspot, I: drivers of population divergence in Restio capensis (Restionaceae). Molecular Ecology. 10.1111/mec.12870

Validity of the findings

Zhang et al. investigate the phylogeography of Amygdalus mongolica, a shrub species from the northwestern China, a region with multiple fragmented environments. The selected species has the potential to shed light on how the last glacial and interglacial climatic fluctuations shaped the demographic patterns of species that occur on this region. As their main result, the authors found that the current phylogeographic structure of A. mongolica is mainly derived from the allopatric divergence of isolated lineages due to expansion of arid environments over the Pleistocene, yielding potential local adaptive differentiation between the fragmented groups.
The authors use genetic markers from plastidial and nuclear genomes, but also implement spatial analyses in their methods. Although the use of so few loci today is seen with skepticism, they were capable of extract relevant information from their limited dataset.
However, I found their manuscript lacks more robust analyses to support some statements. Thus, to better support their results about the restricted gene flow between western and eastern groups I would recommend the implementation of demographic analyses that explicitly test it.

Additional comments

Minor issues:
• The Introduction is quite small, lacking a more robust rationale of the background of the manuscript. Can you provide more details about the studied region? More evolutionary studies developed throughout these mountains? What are the geological, palynological data that support the view that those mountains weren't covered by an ice sheet over the lgm?
• L15-16 – Amygdalus mongolica, a relict and … | Amygdalus mongolica is a relict and …
• L45 – have caused drier climates … | Led to a drier climate, yielding a mosaic of fragmented landscapes
• L46 – to the shrink … | to the shrink of what?
• L46-49 – excessive use of ‘fragment’. Also, this sentence is quite confused. fragmented landscape drove fragment distribution restricting gene flow between fragmentations?
• L66-67 – a Tertiary Miocene relic plant of the Ancient Mediterranean … | Can you provide a reference for this statement?
• L90 – Remove “According to this study”
• L100-101 – which containing an abundance of genetic variation… | Can you provide a reference for this statement?
• L122 – defined groups | which groups?
• L115 and L125 – please, cite R accordingly.
• L224 – mainly distribute | are mainly distributed
• L237 - I wouldn't say that 0.65 is a high posterior value, as stated in your figure 4. Can you inform why did you choose such threshold?
• L249 – And | Besides
• L249 - Bayesian skyline plot (BSP) result was also consistent with species expansion (Fig. 6). | Was it? The panels of figure 6 do not show any postglacial expansion, except maybe for the overall analysis using ndna
• L331-345 - The conservation approach, although important, seems to be a little disconnected from the text.

Reviewer 2 ·

Basic reporting

The manuscript is in general understandable, however some sections are not clear. The Introduction has the right amount of information, while Results need a more detailed explanation. Some Figures have good quality, however, figures 3 and 7 need to be reformatted and/or are not properly described.

Most of the software references are wrong.

Genbank accession numbers do not correspond to the studied species, this should be updated in NCBI or explained in the manuscript.

Experimental design

Research questions are well defined and relevant. The proposed analyses are in accordance with the objectives. The number of markers, the sample number, the analyses in general fulfill the PeerJ standards. Methods are well described and seems to be reproducible.

Overall, analyses are adequate, however some suggestions are listed below.

Validity of the findings

The findings and their interpretation are more or less well presented. However, some results need to be explained. For example, there is no mention in Results about gene flow, and the genetic landscape figure is not described.

The conclusions are connected to the objectives, and apparently supported by the results.

I believe that this work has relevant results. However, the manuscript needs some work, and some parts are overstated and should be reconsidered. For example, in line 246: "postglacial range expansion had been demonstrated in the total populations" while this is in contradiction with the previous results, please avoid the use of this kind of expressions.

Nevertheless, I consider that this work is an important contribution to the management of an endangered species. The proposal of protection areas gives the manuscript practical recommendations.

Additional comments

Consider to change the order of Results. First present the distribution of the haplotypes and then the genetic structure.

Aside to Barrier, consider to use the SAMOVA progam (http://cmpg.unibe.ch/software/samova2/) to statistically identify the number of genetic clusters.

The gene flow estimates were not presented in Results. Also, for the estimation of gene flow use a more robust method like migrate-n (https://peterbeerli.com/migrate/).

The authors state (Lines 212-214): "The genetic landscape shape interpolation surface plots of cpDNA and nDNA sequences indicated significant genetic divergence
occurred between the Western and Eastern regions of A. mongolica (Fig. 7)" What "significant genetic divergence" means? Based on that figure how did you get to this conclusion?

Change the order of the Figures as Fig. 7 is presented before Fig. 4.

Which tree-visualization software did you use?

How heterozygous sites for nuclear genes were verified and codified?

Please present the maps potential distribution based on MaxEnt as supplemental material.


Specific comments

Line 109. Check the ClustalX reference. You can see this paper to corroborate software's year and version: Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., & Thompson, J. D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic acids research, 31(13), 3497-3500.

Line 114. This reference is for Arlequin not for DNAsp, please correct.

Line 118. This reference is for TCS not for HAPLONST. HAPLONST site (http://​www.pierroton.inra.fr/genetics/ labo/Software/index.html)

Line 120. The correct reference is "Slatkin, M. (1985). Gene flow in natural populations. Annual review of ecology and systematics, 16(1), 393-430."

Line 121. There should be specified in methods how the groups were defined for AMOVA. Actually, this should be done also for gene flow an the ht and hs

Line 123. The reference for Network is missing.

Line 125. The reference is wrong.

Line 139. The reference for MEGA X is wrong, please check the software manual.

Lines 140, 144, 166. These references are wrong.

Line 154. I believe that this paragraph should be in line 157.

Line 171. Missing reference.

Line 207. Use lower case for HT and HS as described in methods.

Please include in the text the confidence intervals for divergence estimates.

Lines 244-250. This results are contradictory, and this should be addressed in Discussion. Check if the Skyline plots are plotted from present to past (that is the default), if so, these behavior suggests a population size contraction. Also, the values of the estimates of the effective sizes along their intervals as well as the time of the population size change should be reported.

Figure 1c and 1d. The polygons represent Delunay triangulations? Please especify.

Figure 3. Although 3D components are visually appealing, their interpretation may be ambiguous due to the rotation of the axis. Please use just two components, and use more plots if more than two components are needed to be plotted.

Figure 4. Add the scale bar and specify the units.

Figure 7. It is not clear how the z-axis should be interpreted. It is scaled? It appears to have negative values as it shows "peaks" and "valleys". This does not make sense as all values should have the same sign.

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