Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae)

Naoto Idogawa; Tomonori Sasaki; Kazuki Tsuji; Shigeto Dobata

doi:10.1371/journal.pone.0246710

Peer Review History

Original SubmissionJanuary 23, 2021
15 Mar 2021 Decision Letter - Nicolas Chaline, Editor PONE-D-21-02452 Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae) PLOS ONE Dear Dr. Idogawa, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. The two referees and I think your study is an important contribution to the ever growing field of alternative reproductive strategies in social insects. Only minor revisions are needed and I would be grateful if you were careful in taking them into account to make the paper even clearer and interesting for the reader. Please submit your revised manuscript by Apr 29 2021 11:59PM. 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If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. [Note: HTML markup is below. Please do not edit.] 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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 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 ****** 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 ****** 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: Idogawa et al. have done a very nice job documenting obligate thelotoky in Monomorium triviale. The work is very thorough using multiple approaches that cover all the bases of what one would want to see in a study of this nature. Analyses of additional microsatellite markers would have made it a little stronger, but the results are very solid as is. I appreciated the phylogenetic analysis given the recent upheaval regarding Monomorium taxonomy, as well as the microbial analysis to rule out a bacterial influence underlying asexual reproduction in this species. This study allows us to add another species to the list of obligate thelotokous ants, most specifically, those with queens that produce both new queens and workers parthenogenetically. The different approaches and the results are clear and easy to follow. It is very well written and I’m confident that it will be of general interest to readers of PLoS ONE. I have only very minor suggestions to help improve the paper. Line 95: consider modifying to “First the queen was immobilized by soaking in 70% ethanol for 3 min.” Line 254: should ref. 26 be ref. 27? Line 282: consider rewording to “derived from the same daughter cell during the first meiotic division are fused to restore diploidy after the second meiotic division.” Similarly line 284 could be reworded to read “different daughter cells derived during the first meoitic division are fused.” Line 286: should read “hymenopteran” as it is used as an adjective here rather than a noun. Line 312: consider replacing “habitat” with “habitats” Line 318: consider replacing “Future” with “Additional” to avoid repetition since the last word of the previous sentence is “future.” Excellent paper! Reviewer #2: The occurrence of clonal reproduction in the ant Monomorium triviale has been regularly mentioned in previous publications, but no supporting data has yet been published. In this manuscript, Idogawa and coauthors demonstrate that Japanese populations of this species reproduce by clonal reproduction using several lines of evidence (dissection of queens' spermatheca, observation of laying by virgin queens, and microsatellite analysis) and that no known parthenogenesis-inducing bacteria could be found in colonies. This is a usefull contribution to the field. The methods are sound and the results mostly support the authors' conclusion. One may regret, however, that no data demonstrating worker sterility is shown or cited (i.e. dissection of workers or rearing of queenless colonies). Besides, the discussion regarding the mode of parthenogenesis employed by M. triviale should be reconsidered. The authors suggest that clonal reproduction may proceed through central fusion automixis based on the observation that heterozygosity at the studied microsatellite is maintained across generations. Yet, this pattern could also result from apomictic parthenogenesis or terminal fusion automixis with selection against homozygosity. Minor comments: - There are some inconsistencies in Table 1 (there are more surviving queens than isolated queens in locality 6) and Table 4 (no locality 1 is not mentioned) - l76-77 and l86-88: That "ethanol-preserved samples" are only mentioned for colonies maintained alive sounds weird. - l300-302: One can be more precise here. Having no mutation in 639 bp of COI sequence translates to an estimated divergence time of no more than 45,000 years (assuming a divergence rate of 3.54% My−1; https://doi.org/10.1093/molbev/msq051). Hugo Darras and Laurent Keller ****** 6. 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. If you choose “no”, your identity will remain anonymous but your review may still be made public. 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: No Reviewer #2: Yes:** Hugo Darras and Laurent Keller [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0246710.r001
Revision 1
24 Mar 2021 Author Response Dear Dr. Chaline, We are very pleased to have your valuable comments on the manuscript entitled “Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae)" (PONE-D-21-02452). Based on the important advice from the two reviewers, we have made corrections as much as possible, and the following revisions have been made. Newly added supporting information S1 File responded to comments from reviewer #2 by confirming complete worker sterility in response to. We hope this revised manuscript could now be acceptable for publication. Sincerely, Naoto Idogawa and Shigeto Dobata Response to Reviewers We appreciate your constructive advice and have incorporated them into our manuscript as much as possible, as described below. In the file derived from the original WORD file, the revised sentences are highlighted, including additional acknowledgement. Lines in your comments indicate those of the old version you have already read, and those in the revised manuscript are indicated by line numbers in the WORD file. Journal Requirements [J-1] Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. I&D: We ensured that our manuscript including file naming meets PLOS ONE's style requirements. [J-2] Please ensure you have included the full name of the authority that approved the sampling sites access and, if no permits were required, a brief statement explaining why. I&D: We added a brief statement in the Materials & Methods (Lines 71) that no specific permission for sampling was required. [J-3] We note that Figure 1 in your submission contain map images which may be copyrighted. (~~) We require you to either (1) present written permission from the copyright holder to publish these figures specifically under the CC BY 4.0 license, or (2) remove the figures from your submission. I&D: In our Figure 1, we used map data from Natural Earth (public domain: http://www.naturalearthdata.com/). We indicate the data source credit in figure legend (line 81-82). [J-4] Please review your reference list to ensure that it is complete and correct. I&D: We checked the reference list as much as possible. Reviewer #1 We highly appreciate your valuable comments. We made the following revision: [1-1] Line 95: consider modifying to “First the queen was immobilized by soaking in 70% ethanol for 3 min.” I&D: We modified the sentence accordingly (line 95). [1-2] Line 254: should ref. 26 be ref. 27? I&D: Thank you for your thorough reading. The citation number has been corrected (line 256). [1-3] Line 282: consider rewording to “derived from the same daughter cell during the first meiotic division are fused to restore diploidy after the second meiotic division.” [1-4] Similarly line 284 could be reworded to read “different daughter cells derived during the first meiotic division are fused.” [1-5] Line 286: should read “hymenopteran” as it is used as an adjective here rather than a noun. I&D: We appreciate your suggestion. Following comments from reviewer #2, we removed this paragraph. [1-6] Line 312: consider replacing “habitat” with “habitats” I&D: We modified the sentence accordingly (line 307). [1-7] Line 318: consider replacing “Future” with “Additional” to avoid repetition since the last word of the previous sentence is “future.” I&D: We modified the sentence accordingly (line 313). Reviewer #2 We highly appreciate your constructive suggestions. We made the following revision: [2-1] One may regret, however, that no data demonstrating worker sterility is shown or cited (i.e. dissection of workers or rearing of queenless colonies). I&D: We added the data supporting obligate worker sterility by dissection as a supporting information. [2-2] Besides, the discussion regarding the mode of parthenogenesis employed by M. triviale should be reconsidered. The authors suggest that clonal reproduction may proceed through central fusion automixis based on the observation that heterozygosity at the studied microsatellite is maintained across generations. Yet, this pattern could also result from apomictic parthenogenesis or terminal fusion automixis with selection against homozygosity. I&D: We agree with your comment, our discussion about the mode of parthenogenesis is too speculative. Therefore, we removed this paragraph. [2-3] There are some inconsistencies in Table 1 (there are more surviving queens than isolated queens in locality 6) and Table 4 (no locality 1 is not mentioned) I&D: Thank you for your thorough reading. We understand that you mentioned Table 3 and 4 and corrected them. [2-4] l76-77 and l86-88: That "ethanol-preserved samples" are only mentioned for colonies maintained alive sounds weird. I&D: We agree with your comment. We modified the sentences (line 76-77 and 87-88). [2-5] l300-302: One can be more precise here. Having no mutation in 639 bp of COI sequence translates to an estimated divergence time of no more than 45,000 years (assuming a divergence rate of 3.54% My−1; https://doi.org/10.1093/molbev/msq051). I&D: We appreciate your suggestion: 1,000,000 * (1/639)/0.0354 ~ 45,000. We added (line 295-296) together with the relevant reference. Attachments Attachment Submitted filename: Response to Reviewers.doc https://doi.org/10.1371/journal.pone.0246710.r002
29 Mar 2021 Decision Letter - Nicolas Chaline, Editor Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae) PONE-D-21-02452R1 Dear Dr. Idogawa, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Nicolas Chaline Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0246710.r003
Formally Accepted
13 Apr 2021 Acceptance Letter - Nicolas Chaline, Editor PONE-D-21-02452R1 Comprehensive analysis of male-free reproduction in Monomorium triviale (Formicidae: Myrmicinae) Dear Dr. Idogawa: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Professor Nicolas Chaline Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0246710.r004

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