Review History


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Summary

  • The initial submission of this article was received on January 28th, 2021 and was peer-reviewed by 3 reviewers and the Academic Editor.
  • The Academic Editor made their initial decision on March 2nd, 2021.
  • The first revision was submitted on May 11th, 2021 and was reviewed by 3 reviewers and the Academic Editor.
  • A further revision was submitted on July 15th, 2021 and was reviewed by the Academic Editor.
  • The article was Accepted by the Academic Editor on July 20th, 2021.

Version 0.3 (accepted)

· Jul 20, 2021 · Academic Editor

Accept

Dear Dr. Garrick and colleagues:

Thanks for revising your manuscript based on the concerns that were raised. I now believe that your manuscript is suitable for publication. Congratulations! I look forward to seeing this work in print, and I anticipate it being an important resource for groups studying southern pine beetle ecology and populations genetics. Thanks again for choosing PeerJ to publish such important work.

Best,

-joe

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

Version 0.2

· Jun 24, 2021 · Academic Editor

Minor Revisions

Dear Dr. Garrick and colleagues:

Thanks for revising your manuscript. Two reviewers are very satisfied with your revision (as am I). Great! However, there are some concerns raised by the third reviewer (a few minor by reviewer 2 as well). Please address these and submit a revision ASAP.

Best,

Good luck with your revision,

-joe

·

Basic reporting

The revised version of the manuscript exhibits no further points that need to be improved or enhanced, as the authors have done a very nice work addressing the points raised previsouly. The manuscript is written in a very clear and unambiguous manner, and the literature references are as required. the

Experimental design

The initial concept/question behind this work is something logical that needs to be resolved, and this is very clearly explained in Introduction (Lines 81-93).
The experimental design behind the analysis of this manuscript is very meticulously designed and performed. In particular, the authors pay much attention to the handling of microsatellites in order to gain the most of them, avoiding any possible flaw might have reduced the clarity of the conclusions.

Validity of the findings

As the use of microsatellites might sometimes produce misleading results, the authors have carefully employed numerous methods and protocols that they use in their analysis to avoid such kind of pitfalls (e.g. Lines 255-256/ Lines 267-278). These additional add-ons significantly support the validity of their findings.

Additional comments

Overall, the manuscript by Garrick and colleagues provides a very thorough and interesting investigation on the intra-population structure of D. frontalis across the eastern US, based on the up-to-date approaches in phylogeographic and phylogenetic analyses. For that, I suggest that the manuscript can now be accepted for publication.

·

Basic reporting

The article is very well written, and gives key information for managing a major insect pest.
I particularly appreciated the presentation of the methods, and the discussion of the results, especially the comparison with previous studies.
The authors have responded to all the comments in the previous review.
I therefore recommend this article for publication.
I have just three minor points to note:
l95-109: this paragraph might have been better placed in the discussion, in the "reconciliation with previous work" section for instance. It would make the introduction shorter, and easier to read. This is only a suggestion, however.
l153-156: it is not clear who sampled the specimens and when.
l224: check grammar

Experimental design

no comment

Validity of the findings

no comment

·

Basic reporting

see below

Experimental design

see below

Validity of the findings

see below

Additional comments

While some of my previous comments were taken into consideration, my impression is that they were done so only superficially. The focus remains highly technical in nature and still does not adequately address the questions at hand. Greater clarity and an improved framing of the study is needed. Doing the same analysis with just more markers seems like a poor justification to undertake this work, especially when the value of these markers is put into question given the framing regarding previous contradictory results. Similarly, highlighting the contribution of this re-examination as a “roadmap” (line 140) seems strange, as eliminating potential alternate explanations for observed results is just good science.

Specific comments
Line 44 – and outbreak dynamics?
Line 53 – suggest adding your research objective/question here (e.g., statement on line 72) and starting a new paragraph to present life history information.
Line 75 – development “and application” of molecular tools?
Line 100 – what is a “biologically meaningful distance estimate” and how does one distinguish from an un-meaningful one?
Line 107 –context and citation needed for reference to rapid evolution
Line 113 – Here you refer to the unexpected absences as the motivating problem, but is there any a priori reason to consider the absence of structure to be more likely than the presence of structure? One could also frame this study to examine the unexpected structure identified in the first study. Is it not plausible that technical errors could have resulted in spurious detection of SGS? Why is the absence of structure so much more suspect than its presence?
Line 121 – “albeit ephemerally” – do you know this for sure? Suggest remove
Line 122 – reference needed for this idea
Line 126 – why “notwithstanding ... panmixia”? You refer to panmixia above as a potential alternate hypothesis. You could have both panmixia and weak markers, no?
Line 131 – “only those loci …” – Precedent for this approach? Reference needed
Line 140 – seems strange to highlight the value of new molecular markers. Suggest re-emphasize conceptual (vs technical) contributions.
Line 185 – the absence of consideration of outbreak dynamics and demography as an explanation for the differences between the two studies suggests to me that my previous comments were only superficially taken into consideration. Although referred to int eh discussion, this concept should be woven into the manuscript more thoroughly. Population connectivity and effective population size vary through time in irruptive species, and both of these factors affect population genetic inference. The focus on uSat number and quality misses the mark and does little to actually address your question.

Version 0.1 (original submission)

· Mar 2, 2021 · Academic Editor

Major Revisions

Dear Dr. Garrick and colleagues:

Thanks for submitting your manuscript to PeerJ. I have now received three independent reviews of your work, and as you will see, the reviewers raised some concerns about the research (and manuscript). Despite this, these reviewers are optimistic about your work and the potential impact it will have on research studying southern pine beetle ecology and populations genetics. Thus, I encourage you to revise your manuscript, accordingly, taking into account all of the concerns raised by all three reviewers.

There seems to mainly be missing comparisons with other relevant studies. These are listed by the reviewers and should be acknowledged and included in your analyses/observations/conclusions. Also, more description of the species is needed, as well as your methodology. Please also expand your observations of the data within a broader ecological context.

Therefore, I am recommending that you revise your manuscript, accordingly, taking into account all of the issues raised by the reviewers.

Good luck with your revision,

-joe

[# PeerJ Staff Note: It is PeerJ policy that additional references suggested during the peer-review process should only be included if the authors are in agreement that they are relevant and useful #]

·

Basic reporting

The manuscript of Garrick et al. provides a very interesting and comprehensive analysis on the populations structure of Dendroctonus frontalis across the eastern United States. The language used describes efficiently the concept, methods and results of this analysis, whereas the authors cite all the necessary lliterature references. I believe however, that the introductory part should be somehow complemented with a few more information regarding D. frontalis itself, before explaining all the previous studies that were done on this species.

Experimental design

The experimental design is really robust. The authors address each approach individually, and explain in details what they will do and why they chose this approach. This works excellently in their case, as they leave nothing vague or questionable, something that facilitates greatly the comprehension of their work. This is further enhanced by providing the settings employed in each software, something that allows the replicate of their analysis. Nevertheless, what I would really like to see included in the Materials and Methods part, are a couple of sentences describing the process used when sampling the D. frontalis individuals. In my opinion, this is important particularly in phylogeographic studies, and should be added, .

Validity of the findings

Following the structure they adopted in the description of the Experimental Design, the authors clearly address each approach, and explain their findings. It is also very important, that their speculation regarding the detection of IBD when only females were included, is learly identified as such, leaving no doubt about that.

Additional comments

The manuscript of Garrick and colleagues provides a very interesting and comprehensive analysis of the population structure of D. frontalis in the eastern United States. The authors adopt a very convenient and reader-friendly format to present the methods used, presenting each approach individually, providing the necessary information therein. This becomes even more important in the next parts (Results and Discussion) as by doing that, they facilitate reader to easily and effectively understand how the authors have reached to these conclusions. The only thing I would like to the authors to add, is some more information regarding D. frontalis in the Introduction, but also some details about the sampling protocol of the individuals analysed.

·

Basic reporting

The article by Garrick et al. assessed several explanations for the absence of spatial genetic structure in a native pest, Dendroctonus frontalis.
The article is well written and includes enough background to demonstrate how the work is relevant for the field and for the management of D. frontalis.

Experimental design

The methods and experimental design are clearly explained. There are many stages of analysis but the structure of the text is very clear. The choice of methods is well justified.

Validity of the findings

The manuscript confirms the lack of discrete population differentiation and isolation by distance in D. frontalis, based on several, complementary methods, and the authors give several explanations for this result.
As indicated by the authors, these results have strong implications for the management of D. frontalis

Additional comments

Perhaps a paragraph should be added in the introduction on the biology of the species, with a focus on the traits that may affect its genetic structure. The authors already mentionned dispersal distances l59-61, but other traits such as temperature tolerance or reproductive mode could also have an influence.

L404-417 - identifying the best-fit value of K : read Janes et al. (2017) and Tsykun et al. (2019) for an illustration of the method.
--> Janes, J. K. et al. The K = 2 conundrum. Mol Ecol 26, 3594–3602, https://doi.org/10.1111/mec.14187 (2017).
--> Tsykun, T. et al. Fine-scale invasion genetics ofthe quarantine pest, Anoplophora glabripennis, reconstructed in single outbreaks. Scientific reports. 9:19436 (2019)

L462-463 – Add a reference like Lombaert et al. (2010) for bridgehead effect, and like Whitney & Gabler (2008) for rapid evolution in introduced species.
--> Lombaert, E. et al. Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One 5:e9743 (2010)
--> Whitney, KD & Gabler, CA Rapid evolution in introduced species, “invasive traits” and recipient communities: Challenges for predicting invasive potential. Divers. Distrib. 14:569-580 (2008)

L508 – see also Roques et al (2012)
--> Roques, L. et al. Allee effect promotes diversity in traveling waves of colonization. PNAS 109 :8828-8833 (2012)

L571-572 – Remove one « Generally »

·

Basic reporting

no comment - see below

Experimental design

no comment - see below

Validity of the findings

no comment - see below

Additional comments

The authors provide a detailed analysis of the population genetic structure of the southern pine beetle in the eastern US with the goal of reconciling different results found in the same system. The manuscript is well written and well-organized.

I have two main concerns about this manuscript.

First, I sincerely appreciate the attention to detail and the well-organized approach that was taken in this manuscript. However, I do have concern that these detailed investigations were not undertaken in the previous analysis and associated publications. The onus should be on an author to explore these types of questions when first reporting on the phenomenon. As written, this is a (well-executed) technical piece of work, however, without much of a conceptual contribution. For that reason, while the science undertaken is acceptable, I question the strategy that is being taken here.

Second, related to conceptual contributions, I was a bit surprised that that main line of inquiry was related to techno/analytical solutions to this problem. The assumption seems that if two different studies found different patterns of spatial genetic structure, then something must be wrong with our molecular markers. Ecological context (i.e., timing and outbreak status) was surprisingly not considered. As indicated above, while I do appreciate the due diligence of verifying that the markers and analytical approach were not at fault, I was surprised that more attention wasn’t given to alternate ecological and demographic explanations.

One very logical explanation from my perspective is that the two studies that precipitated this analysis were conducted at different points in time during and outbreak (i.e., 2011 vs. 2019). This idea is mentioned near the end of the MS (line 580 +). Given that you eliminated all other possible explanations, I feel that this explanation should be given greater attention. The spatial genetic consequences of cyclic and irruptive populations are not yet well understood, but I feel that you have likely landed on the most plausible answer in your comment about existing structure being “overwritten” (line 584). Your work may not be “complicated” by this issue of different timings of sampling, but in fact may be driven by them. Please see James et al (2015) and Larroque et al (2019) in this regard. I encourage you to explore this idea in more detail to not only better describe the interesting differences in SGS in D. frontalis at different points of time, but also to add further conceptual content and rigour to this work.


James PMA, Cooke B, Brunet B, Lumley L, Sperling FAH, Fortin M-J, Quinn V, Sturtevant BR. 2015. Life-stage differences in spatial genetic structure in an irruptive forest insect: Implications for dispersal and spatial synchrony. Molecular Ecology. 24(2): 296-309.

Larroque J, Legault S, Johns R, Lumley L, Cusson M, Renaut S, James PMA. 2019. Temporal variation in spatial genetic structure during population outbreaks: distinguishing among different potential drivers of spatial synchrony. Evolutionary Applications 12(10): 1931-1945

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