PONE-D-19-16483

Reconstructing the population history of the sandy beach amphipod Haustorioides japonicus using the calibration of demographic transition (CDT) approach

PLOS ONE

Dear Dr. Sakuma,

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Tzen-Yuh Chiang

Academic Editor

PLOS ONE

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 [This study was partly supported by “A project for development of assessment methods for the coastal environment” funded by the Ministry of Agriculture, Forestry and Fisheries, and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (25340114 and 15H02265).]. 

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4. We noted in your submission details that a portion of your manuscript may have been presented or published elsewhere. [Some nucleotide sequences (see Table S1) used in the present study were published previously and available online. The aim of the present study and thus analytical procedures are different from that of the previous one and also, we used additional sequences. This submission therefore does not constitute dual publication.]

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Sakuma and colleagues have reconstructed the demographic history of several populations of the amphipod Haustorioides japonicus using an approach based on demographic transition from an ancient epoch of constant population size to a modern epoch of rapid increase. The rapid population increase is assumed to have been triggered by warming temperatures following the Last Glacial Maximum. This approach is very interesting and has rarely been explored. As such, the present study is important as it explores the strengths and weaknesses of the method. The manuscript is well written, concise, the language is very good and the figures are of good quality. Overall, the analyses are done properly, although some clarifications are needed here and there. I have some remarks that should improve the presentation of the paper.

Line 41 “change of rate temperature” should be “rate of temperature change”.

Line 147. I recommend the authors to also use the R2 test (implemented in DnaSP) since it is more sensitive, especially regarding small sample sizes (Ramos-Onsins, S.E., Rozas, J., 2002. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19, 2092–2100).

Line 154. “we built TEMs based on the whole sequence of the population to which the Tohoku population was assigned”. This needs to be rephrased as it is not clear. Does it mean that TEMs were build using all individuals from the NWP populations?

Line 156. Why did the authors not consider a strict clock as well for the BF comparisons?

Line 163. “9000 mutation values from the best model were obtained”. Please specify exactly to what parameter this refers to from the BEAST output file.

Lines 165-169. Please give more details here. What packages and their versions were used for these analyses?

Line 171. “inferred the history” should be “inferred the demographic history”. Write what BSP means when mentioned the first time. It is a bit confusing because the authors mention that they inferred the history of the Tohoku population, when in fact they analyzed this population together with the other NWP populations. This is made clear only in the results, but it should be clear here as well. Also in the BSP analyses it is not clear what kind of clock was used (strict vs relaxed). The authors mention the strict clock only in the second model based on the 1% evolutionary rate.

The authors compare their obtained rate with a phylogenetic (interspecific) rate of 1%. Although I see the use of such comparison, I do not see the point of the arbitrarily chosen 1% rate. I would recommend the authors to compare their intraspecific rate with interspecific (phylogenetic) rates that have been inferred for other crustaceans (e.g. Knowlton & Weigt 1998 https://doi.org/10.1098/rspb.1998.0568) and recently even amphipods (Copilas-Ciocianu et al. 2019 https://doi.org/10.1007/s13127-019-00401-7).

The authors should also clarify what they mean by “rate”. There is substitution rate and divergence rate (which is 2x substitution rate). In their MS, I suppose that the authors refer to the substitution rate. There is confusion in the literature about this, and that is why there should be more clarity (Schenekar & Weiss 2011 doi:10.1038/hdy.2011.48).

Line 325. Here the authors should also mention that several studies have shown fast intraspecific rates in crustaceans as well (Audzijonyte&Vainola 2006 http://dx.doi.org/10.1111/j.1365-294X.2006; Crandall et al. 2012 http://dx.doi.org/10.1093/molbev/msr227).

Reviewer #2: I found your work on the sandy beach amphipod Haustorioides japonicus really interesting. It represents an important and interesting contribution as it shows, for the first time, the power of the calibration of demographic transition approach and the importance of using an adequate evolutionary rate in an amphipod species.

In general, the organization of the manuscript is satisfactory and its easy reading. The TITLE clearly reflects the contents. The ABSTRACT is sufficiently informative and has a correct length. The INTRODUCTION is very interesting, clear and concise, and contains enough background to put the reader in context. The statement of the objective is adequate and appropriate. MATERIAL AND METHODS are clearly explained, being sufficiently informative to allow replication. The analyses are properly detailed, and they are solid. The RESULTS are clearly presented and described in a logical order, and their interpretation and posterior discussion are justified by the data and consistent with the objectives. The DISCUSSION and CONCLUSIONS are very clear and well organized. Authors explain properly their results obtained with many adequate references. Finally, the English is adequate.

Overall, I think the paper is interesting and worthy of publication. I think that this paper could be accepted in PLOS ONE as the subject of the manuscript falls within the scope of the journal. Some suggestions and corrections were made to improve it (see below) that should be relatively easy for the authors to fix. So, I consider that this manuscript is acceptable for publication after minor revisions.

IMPORTANT:

According to the “World Register of Marine Species” (WoRMS) database, Haustorioides japonicus is an unaccepted species. The accepted species name corresponds to “Eohaustorioides japonicus (Kamihira, 1977)”. Therefore, the authors must correct this along the whole manuscript including the corresponding title and the abstract.

INTRODUCTION

- Line 86: “(Dogielinotidae: Amphioda)”. The Order name must be before the Family name. Therefore, the authors should place “Amphipoda” before “Dogielinotidae”.

- Line 95: “genetically distinct”. Genetically distinct from what? The authors should clarify this to avoid confusion.

- Line 97: “BSP”. What does BSP mean? Bayesian Skyline Plot? When you use an abbreviation, its meaning should be specified the first time it appears in the manuscript. Therefore, the authors should include this information.

- Line 97: “genealogy”. Please, include “of the sandy amphipod Eohaustorioides japonicus”, just to make it clear.

MATERIALS AND METHODS

- Line 109 - 110: “three sandy beaches in the Tohoku region and two sites along the coast of Hokkaido”. In the present study, according to Figure 1 legend (empty circles) and locations in Table 1, only one location was sampled along the coast of Hokkaido (site 4, Usu). Therefore, the authors should replace “two sites along…” with “one site along…”

- Line 111: “parts”. Which parts were preserved? Did the authors preserve some specific parts for some reason? Please, specify this.

- Line 115: Please, include a “a” after “using”.

- Line 135: I will include a sentence saying that sequences were deposited in GenBank (accession numbers: LC474498–LC474506) (S1 Table).

- Line 137: “The 300 sequences”. Sequences used by Takada et al. [13] were 105 and not 300, as the authors can see in the Table S1 of Takada et al.’s paper. The authors should correct this.

RESULTS

- Line 207: “(site 7)”. The authors should include “Fig 1” after “(site 7)” to ensure that readers understand exactly which location is talking about.

- Line 211: “two populations”. Really, NWP is not only one population but a group of them. Therefore, I think, the authors should replace “two populations” with “two group of populations”. The same should be modified in Table 2 captions.

DISCUSSION

- Line 289: “Littorina saxatilis”. The authors should include the authority of this taxon.

REFERENCES:

- Line 412: Please, remove the comma after “Kamihira”

- Line 418: Please, remove the comma after “Kamihira”

- Line 465: “Haustorioides japonicus” must be in italics. Please, change it.

FIGURES AND TABLES:

- Figure 1: It is clear and appropriate for the data being presented. However, I think, it is necessary to include/specify two things:

o According to the manuscript, Tohoku region is located along the Pacific coast of northeastern Honshu Island, Japan. However, this region is not clearly indicated in the Figure. As this region is very important in the present study, it should be clearly indicated to put the readers in context and to ensure that they understand exactly which region corresponds to Tohoku region.

o This Figure is extremely similar to Figure 1 of Takamada et al. [13]. In fact, the maps used are the same. I think, the authors should include in the legend something like: “Modified from Takada et al. [13]”.

- Figure 2: In the Figure 2 (A) appears a total of 16 haplotypes. However, in Table S1 and in the manuscript (for example, line 194) is stated the existence of 15 haplotypes, not 16. Specifying, the haplotype Hja_033 appears in Figure 2 but is missing in Table S1. Could the authors explain this fact? Please, correct this properly in the paper.

- Table 1: Please, include “(n)” after “sample size”

- Table 2: Please, replace “two populations” with “two group of populations” in Table legend. See comments for Line 211.

- S1 Table: “total number (n)”. Total number of individuals? Please, indicate this in the Table caption.

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Reviewer #1: Yes: Denis Copilas-Ciocianu

Reviewer #2: Yes: M. Pilar Cabezas

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Reconstructing the population history of the sandy beach amphipod Haustorioides japonicus using the calibration of demographic transition (CDT) approach

PONE-D-19-16483R1

Dear Dr. Sakuma,

We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements.

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With kind regards,

Tzen-Yuh Chiang

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: Authors perfectly addressed the comments made by the two reviewers. The manuscript is now acceptable for publication.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Denis Copilas-Ciocianu

Reviewer #2: Yes: M. Pilar Cabezas