Post-mating parental behavior trajectories differ across four species of deer mice

Mehdi Khadraoui; Jennifer R. Merritt; Hopi E. Hoekstra; Andres Bendesky

doi:10.1371/journal.pone.0276052

Peer Review History

Original SubmissionAugust 16, 2022
1 Sep 2022 Decision Letter - Andrey E Ryabinin, Editor PONE-D-22-22997Post-mating parental behavior trajectories differ across four species of deer micePLOS ONE Dear Dr. Bendesky, 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. While the two reviewers are positive about your study, they clearly outline their concerns with the manuscript. If you feel that you can fully address these concerns, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Oct 16 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. 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The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section. 3. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. 4. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references.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 If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.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: Partly 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: In this interesting manuscript the authors conduct detailed analyses of parental behavior in four species of Peromyscus that differ in their social organizations. The authors show that in two species (P. polionotus and P. californicus) that males engage more parental behavior than males in P. leucopus or P. maniculatus. Although parental behavior in these species have been studied previously, the paper has several strengths. The same procedure is used for all four species, four time points are observed, mating is carefully observed, and the authors include a diversity of behavior variables. There is one important weakness in that males and females are not tested in the same way even though they are directly compared. Although not ideal, I believe the authors could address this in the discussion and the abstract to make a good contribution to the literature. The main issue is that behavior testing protocol is a little unconventional. The females are tested in the home cage first while the males are moved to a new cage (with pups if they are present). Then, the male is tested in a new cage. Even though the males have 60 minutes of habituation in the new cage, the transfer to the new cage is stressful. Thus as written, the females are tested in the home cage and the males in a novel environment. The authors need to consider the potential impact of stress via the handling of their procedure may have on behavior. Simply removing a wire cage lid from a cage can have a strong inhibitory effect on parental behavior in P. californicus (Kowalczyk et al. 2018). It’s possible the handling may have contributed to the lack of parental care in virgin P. californicus in contrast to work from the Saltzman lab which has observed more paternal behavior in virgin P. californicus (eg Nguyen et al 2020) (although Gubernick reported more infanticide in virgin males). Physiological stress responses and behavioral responses to novelty have been studied in some of these species, but I’m not aware of all four being directly compared to each other. The authors need to consider the possibility that the reason why P. polionotus show male parental behavior sooner is that those males are less sensitive to novel environments than P. californicus. This should be addressed in the discussion and the abstract. It looks like some of the references are mixed up. On line 40 the references for the mice being nocturnal and mating at night are 28 and 33 which are about social organization of polionotus and californicus. The quality of the supplementary figures is not very good. Even when I zoomed in the graphs were very pixelated. I couldn’t tell if this was a problem with the journal website or the original figures. Reviewer #2: In this manuscript, the authors characterized parental behavior in 4 species of mice from pre-mating to post-parturition. The species of mice they studied varied by mating system (monogamous vs. promiscuous) as well as species-typical dispersal patterns and territory size. Their study found results for female parental behavior that supports previous findings in the literature, yet they also provide novel data about male parental trajectories in these species. The characterization of paternal care patterns in these species provides a novel and valuable contribution to the field. The manuscript was well-written and appropriately succinct. I have only 2 minor comments. Methods - Was cause of death for the deceased 1st litters examined? It just seems like a mark against parents if they killed their pups… but if the cause of death was dehydration or malnutrition, then it would suggest a health issue such that perhaps the mother wasn’t producing milk. The latter cause of death wouldn’t be concerning for this dataset, but the former (i.e., killing pups) may have some implications for species-typical parenting. Discussion - Does the habitat differ between white-footed and deer mice? Can the nest building skills be attributed to what these mice evolved to use for nesting material in the wild (i.e., does one species actually build nests using grass/pine needles/etc. and another species just burrows in dirt or lives in hollowed out parts of logs, never really building nests)? ****** 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: No ******** [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.0276052.r001
Revision 1
18 Sep 2022 Author Response Below you will find detailed answers (in red) to the Journal requirements and to the reviewers’ comments below. Journal requirements When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf We revised our manuscript to meet the requirements from these two links. Our first page now matches the required format, and the names of our supplemental files have been changed as well. 2. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section. We provide correct grant numbers in the ‘Funding Information’ section. 3. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. IACUC approval was already included in the Methods section. 4. Please review your reference list to ensure that it is complete and correct. 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. We have now reviewed the list of references to ensure it is complete and correct. Reviewer 1 In this interesting manuscript the authors conduct detailed analyses of parental behavior in four species of Peromyscus that differ in their social organizations. The authors show that in two species (P. polionotus and P. californicus) that males engage more parental behavior than males in P. leucopus or P. maniculatus. Although parental behavior in these species have been studied previously, the paper has several strengths. The same procedure is used for all four species, four time points are observed, mating is carefully observed, and the authors include a diversity of behavior variables. There is one important weakness in that males and females are not tested in the same way even though they are directly compared. Although not ideal, I believe the authors could address this in the discussion and the abstract to make a good contribution to the literature. The main issue is that behavior testing protocol is a little unconventional. The females are tested in the home cage first while the males are moved to a new cage (with pups if they are present). Then, the male is tested in a new cage. Even though the males have 60 minutes of habituation in the new cage, the transfer to the new cage is stressful. Thus as written, the females are tested in the home cage and the males in a novel environment. We thank reviewer 1 for this relevant comment. We have now addressed this weakness in the Discussion section (lines 405-408). We acknowledge that our testing protocol may have influenced sex differences in parental behavior. We designed our testing protocol in this manner to reduce the stress on females and their litters that would have been incurred if we had to individually test the male in his home cage in the absence of the female. We also believe that the long habituation phase of 60 minutes mitigated possible effects on male behaviors. The authors need to consider the potential impact of stress via the handling of their procedure may have on behavior. Simply removing a wire cage lid from a cage can have a strong inhibitory effect on parental behavior in P. californicus (Kowalczyk et al. 2018). It’s possible the handling may have contributed to the lack of parental care in virgin P. californicus in contrast to work from the Saltzman lab which has observed more paternal behavior in virgin P. californicus (eg Nguyen et al 2020) (although Gubernick reported more infanticide in virgin males). Physiological stress responses and behavioral responses to novelty have been studied in some of these species, but I’m not aware of all four being directly compared to each other. The authors need to consider the possibility that the reason why P. polionotus show male parental behavior sooner is that those males are less sensitive to novel environments than P. californicus. This should be addressed in the discussion and the abstract. Reviewer 1 highlights inconsistencies in the literature about the effect of stress via handling on behavior of different species or groups. This is an important point, and we have now addressed this possible effect in our discussion (lines 401-405). We have also added the references mentioned by reviewer 1 to show that short habituation phases after cage manipulations can have an effect on behavior. We expect that 60 minutes of habituation (4 to 6 times longer than the references mentioned by the reviewer) were enough to mitigate the effects of stress. It looks like some of the references are mixed up. On line 40 the references for the mice being nocturnal and mating at night are 28 and 33 which are about social organization of polionotus and californicus. We have now revised our references and ensured that they corresponded to the points made throughout the paper. The particular references highlighted by reviewer 1 were changed to a new reference. The quality of the supplementary figures is not very good. Even when I zoomed in the graphs were very pixelated. I couldn’t tell if this was a problem with the journal website or the original figures. We have checked our supplementary figure (S7) and made sure our file was of high resolution. We’ve noticed Plos PDFs for reviewers often have a low resolution figure with a link to the high resolution version. Reviewer 2 In this manuscript, the authors characterized parental behavior in 4 species of mice from pre-mating to post-parturition. The species of mice they studied varied by mating system (monogamous vs. promiscuous) as well as species-typical dispersal patterns and territory size. Their study found results for female parental behavior that supports previous findings in the literature, yet they also provide novel data about male parental trajectories in these species. The characterization of paternal care patterns in these species provides a novel and valuable contribution to the field. The manuscript was well-written and appropriately succinct. I have only 2 minor comments. Methods Was cause of death for the deceased 1st litters examined? It just seems like a mark against parents if they killed their pups… but if the cause of death was dehydration or malnutrition, then it would suggest a health issue such that perhaps the mother wasn’t producing milk. The latter cause of death wouldn’t be concerning for this dataset, but the former (i.e., killing pups) may have some implications for species-typical parenting. We have not examined the cause of death of lost litters, since this is very challenging. Dead pups can die from infanticide or be injured or eaten after death from other causes. In some cases, we could not be sure there had been a litter at all, as young parents can eat their young very soon after birth and leave no trace. This point is now addressed under Experimental timeframe and pairing in the Materials and Methods section (lines 165). Discussion Does the habitat differ between white-footed and deer mice? Can the nest building skills be attributed to what these mice evolved to use for nesting material in the wild (i.e., does one species actually build nests using grass/pine needles/etc. and another species just burrows in dirt or lives in hollowed out parts of logs, never really building nests)? The habitat preferences of P. leucopus and P. maniculatus bairdii partially overlap. While interspecific differences in the habitat adaptations and nesting-material use of our species may have had an effect on our findings, we preferred to keep speculation at a minimum in the discussion. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0276052.r002
28 Sep 2022 Decision Letter - Andrey E Ryabinin, Editor Post-mating parental behavior trajectories differ across four species of deer mice PONE-D-22-22997R1 Dear Dr. Bendesky, 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, Andrey E Ryabinin, Ph.D. 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 ******** 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: (No Response) ****** 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: nice revision, this is a great paper. It's strange that this journal requires 100 character response when you are recommending acceptance. Reviewer #2: (No Response) ****** 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. 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: No ******** https://doi.org/10.1371/journal.pone.0276052.r003
Formally Accepted
7 Oct 2022 Acceptance Letter - Andrey E Ryabinin, Editor PONE-D-22-22997R1 Post-mating parental behavior trajectories differ across four species of deer mice Dear Dr. Bendesky: 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 Dr. Andrey E Ryabinin Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0276052.r004

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