Insecticide resistance and species diversity in Anopheles gambiae s.l. in Côte d’Ivoire

Rosine Z. Wolie; Alphonsine A. Koffi; Joseph Chabi; Ludovic P. Ahoua Alou; Eleanore D. Sternberg; Kouakou P. M. Kouame; Florent H. A. Yapo; Soromane Camara; Amal Dahounto; Innocent Z. Tia; Welbeck A. Oumbouke; Kallista Chan; Oulo N’Nan-Alla; Raphael N’Guessan

doi:10.1371/journal.pone.0332497

Peer Review History

Original SubmissionJanuary 1, 2025
30 Jan 2025 Decision Letter - Adekunle Bakare, Editor Dear Dr. Wolie, 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. Please submit your revised manuscript by Mar 16 2025 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 . When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. 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The grant aimed to strengthen malaria vector surveillance in Côte d’Ivoire, specifically addressing the genetic diversity and gene flow data gaps in insecticide-resistant Anopheles gambiae.” Please state what role the funders took in the study. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." If this statement is not correct you must amend it as needed. Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. 6. In the online submission form, you indicated that “The data supporting the conclusions of this manuscript are included within the text and are available from the corresponding author upon reasonable request.” All PLOS journals now require all data underlying the findings described in their manuscript to be freely available to other researchers, either 1. In a public repository, 2. 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Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. 9. 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? 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 Reviewer #1: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English??> Reviewer #1: Yes Reviewer #2: Yes ****** Reviewer #1: The manuscript is well structured and written. My only comments are that it might have been a more valuable study if further investigation into the specifics of metabolic resistance was investigated e.g. which P450s are associated with the resistance recorded rather than the more general finding associated with the use of PBO. Also, data on the susceptibility to newer insecticides that are being introduced for vector control uses such as chlorfenapyr, clothianidin and broflanilide might have been an interesting addition. Reviewer #2: This study is about mosquito diversity and the distribution of resistance mechanisms among malaria vectors in three ecological areas in Côte d’Ivoire. The overall manuscript was very well written in easy English, with good results and important recommendations. I only have minor reviews which if addressed could help the readers to better understand the study. Minor reviews 67 Please rephrase this sentence to make clearer when PBO was conducted 69-70 ‘target site mechanisms (Kdr L1014F and Ace-1R G119S) determined using PCR’ is there a ‘were’ that is missing? 75 please delete ‘collected’ 76-77 ‘in the savannah area (97-100% of collected mosquitoes)’ and in all the result part of the background please change the range to the mean of the proportion with the confidence interval (CI). For example ‘in the savannah area (97.9%, 95% CI [96.2-99.7]) or simply rephrase 96-97 please add some references about the seven species 99 Please write some key findings of these authors in the text 108 the introduction is well written however it lacks some related literature that had already shown by their results the importance of addressing insecticides resistances patterns according to species level in Côte d’Ivoire and other country of Africa. Please add some of them. It is not clear what the authors mean by ‘adequately’, please be more precise 109-110 add some references from the country of study 100, 122, 167 italic for malaria vector name Anopheles, please check throughout the paper Method/Result In the method section, it is important to mention how long the CDC light trap were installed (one week, one month, two days per week for two months, …?). This allows the reader to know the frequency of collection that allowed the authors to have the number of mosquitoes mentioned in the part of the results and help in terms of reproducibility of the study 129-132: ‘Adult mosquitoes were collected using CDC light traps, which were set for two to three nights per study site’. Does it mean that for each of the six sites chosen for this study just one CDC light trap was installed? Were they installed simultaneously in the sites or in different period? When talking about the three different locations (132) the authors only mentioned ‘near a bed and outside on the veranda’ is there any other location missing? Does it mean that there were three CDC light traps per house? This part of the method needs more details 162: the authors stated that 504 mosquitoes were chosen randomly to conduct species ID. The selection was random between each ecological region/ each method of capture? How did the authors proceed to avoid any bias? Please be more explicit 173 the authors mentioned odds ratios however throughout the manuscript there was no mention of OR. Please have a look 179 please add a link for the software 213-214 repetition of ‘both’ please delete one of them Discussion 241-243 It was not the first time that hybrids were identified in Aboisso please check this reference https://doi.org/10.1371/journal.pone.0297604 243-247 you can review this part of the discussion considering the number of hybrids they found in this study https://doi.org/10.1371/journal.pone.0297604 or any other study that you can find from Aboisso, considering the date of collection and also the method of capture 259 Please add other references as you mentioned many other parts of Côte d’Ivoire 262-265. Anything about the low number of mosquitoes collected in the savannah region compared to the others? Don’t the authors think that the number of localities sampled by ecological regions could have influenced difference in terms of number of mosquitoes collected and the composition of mosquito species? Please address this either in the main discussion or in the limits of the study I would like also the authors to address the limitations of the study regarding the period of collection July-October, because maybe the results would have been different when talking about species distribution in other periods of the year 487 Table 1. please add the stage of mosquitoes (larval and adult) in the title to make it more explicit 489 In the legend of the table 1 please be clearer about what type of significance the letters and numbers shown. For example, for each species in each column is the same letter shows that there is not a significant difference between method of capture? What about the numbers? 500 `Table’ instead of ‘tableau’ 501 there is a ‘t’ missing in adult ‘catches’ in the table 2 503 Again as for the table 1, in the legend ‘For each mutation in each species, values in the same column sharing the same superscript letters do not differ significantly’ it is not clear what are the variables that the authors were addressing. Is it a significant difference between method of capture? Between ecological areas? Please address each parameter (letter/number) and add this information to the legend Figure 2. instead of proportion (%) you can write proportion% (number) Title of Figure 3. repetition of ‘synergist’ Legend of Figure 3. Please address the abbreviations as they are written in the figure. Repetition of what the errors bars indicate ****** 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. 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Revision 1
29 Aug 2025 Author Response Response to reviewers and journal requirements Responses to journal editorial 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 Responses 1: We corrected the formatting of all section titles, updated the corresponding author asterisk, edited the inline equation, and revised the table titles, column headers, and row labels to comply with PLOS ONE guidelines. 2. In your Methods section, please provide additional information regarding the permits you obtained for the work. Please ensure you have included the full name of the authority that approved the field site access and, if no permits were required, a brief statement explaining why Responses 2: We clarified in the Methods section that national ethical approval, together with written informed consent from community members, served as the official authorization to conduct mosquito collections at all study sites (Lines 206-208.). 3. Please note that funding information should not appear in any section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript. Responses 3: We have removed the funding information from the main manuscript, as requested. It is now included only in the Funding Statement section of the online submission form (Lines 346). 4. Please note that funding information should not appear in any section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript. Responses 4: This point duplicates the previous request. As stated above, we have removed the funding information from the main manuscript. 5. Thank you for stating the following financial disclosure: “This work was supported by a grant awarded to the Institut Pierre Richet / Institut National de Santé Publique, Côte d’Ivoire, from the Bill & Melinda Gates Foundation (OPP1210335) through the Pan African Mosquito Control Association (PAMCA). The grant aimed to strengthen malaria vector surveillance in Côte d’Ivoire, specifically addressing the genetic diversity and gene flow data gaps in insecticide-resistant Anopheles gambiae.” Please state what role the funders took in the study. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." If this statement is not correct you must amend it as needed. Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. Responses 5: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We will include this statement in the cover letter, as requested. 6. In the online submission form, you indicated that “The data supporting the conclusions of this manuscript are included within the text and are available from the corresponding author upon reasonable request.” All PLOS journals now require all data underlying the findings described in their manuscript to be freely available to other researchers, either 1. In a public repository, 2. Within the manuscript itself, or 3. Uploaded as supplementary information. This policy applies to all data except where public deposition would breach compliance with the protocol approved by your research ethics board. If your data cannot be made publicly available for ethical or legal reasons (e.g., public availability would compromise patient privacy), please explain your reasons on resubmission and your exemption request will be escalated for approval. Responses 6: We have revised the Availability of data and materials section in the manuscript to align with PLOS ONE data sharing policy. It now states that the data are included in the text and that the underlying datasets will be deposited in a public repository and made fully accessible upon acceptance. 7. We note that Figure 1 in your submission contain map/satellite images which may be copyrighted. All PLOS content is published under the Creative Commons Attribution License (CC BY 4.0), which means that the manuscript, images, and Supporting Information files will be freely available online, and any third party is permitted to access, download, copy, distribute, and use these materials in any way, even commercially, with proper attribution. For these reasons, we cannot publish previously copyrighted maps or satellite images created using proprietary data, such as Google software (Google Maps, Street View, and Earth). For more information, see our copyright guidelines: http://journals.plos.org/plosone/s/licenses-and-copyright. We require you to either (a) present written permission from the copyright holder to publish these figures specifically under the CC BY 4.0 license, or (b) remove the figures from your submission: a. You may seek permission from the original copyright holder of Figure 1 to publish the content specifically under the CC BY 4.0 license. We recommend that you contact the original copyright holder with the Content Permission Form (http://journals.plos.org/plosone/s/file?id=7c09/content-permission-form.pdf) and the following text: “I request permission for the open-access journal PLOS ONE to publish XXX under the Creative Commons Attribution License (CCAL) CC BY 4.0 (http://creativecommons.org/licenses/by/4.0/). Please be aware that this license allows unrestricted use and distribution, even commercially, by third parties. Please reply and provide explicit written permission to publish XXX under a CC BY license and complete the attached form.” Please upload the completed Content Permission Form or other proof of granted permissions as an "Other" file with your submission. In the figure caption of the copyrighted figure, please include the following text: “Reprinted from [ref] under a CC BY license, with permission from [name of publisher], original copyright [original copyright year].” b. If you are unable to obtain permission from the original copyright holder to publish these figures under the CC BY 4.0 license or if the copyright holder’s requirements are incompatible with the CC BY 4.0 license, please either i) remove the figure or ii) supply a replacement figure that complies with the CC BY 4.0 license. Please check copyright information on all replacement figures and update the figure caption with source information. If applicable, please specify in the figure caption text when a figure is similar but not identical to the original image and is therefore for illustrative purposes only. The following resources for replacing copyrighted map figures may be helpful: USGS National Map Viewer (public domain): http://viewer.nationalmap.gov/viewer/ The Gateway to Astronaut Photography of Earth (public domain): http://eol.jsc.nasa.gov/sseop/clickmap/ Maps at the CIA (public domain): https://www.cia.gov/library/publications/the-world-factbook/index.html and https://www.cia.gov/library/publications/cia-maps-publications/index.html NASA Earth Observatory (public domain): http://earthobservatory.nasa.gov/ Landsat: http://landsat.visibleearth.nasa.gov/ USGS EROS (Earth Resources Observatory and Science (EROS) Center) (public domain): http://eros.usgs.gov/# Natural Earth (public domain): http://www.naturalearthdata.com/ Responses 7: Thank you for this important clarification. The map was generated using QGIS v2.14.19 with GPS coordinates of the mosquito collection points. The base layers were obtained from the Centre de Cartographie et de Télédétection (CCT) of the Bureau National d’Études Techniques et de Développement (BNETD) in Côte d’Ivoire. All vector layers, including vegetation types and administrative boundaries, were digitized by the authors using publicly available sources. No copyrighted or proprietary maps (e.g., Google Maps) were used. This information has been added to the revised Methods section and the revised figure has been included in the resubmission (Lines 128-131). 8. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. Responses 8: We have added a Supporting information section at the end of the manuscript, including full captions for each supplementary figure, table, and document, in accordance with PLOS ONE guidelines (Lines 545-558). 9. 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. Responses 9: We have reviewed the reference list and confirm that it is complete and up to date. No retracted articles are cited in the manuscript. Responses to Reviewers’ comments: 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: The manuscript is well structured and written. My only comments are that it might have been a more valuable study if further investigation into the specifics of metabolic resistance was investigated e.g. which P450s are associated with the resistance recorded rather than the more general finding associated with the use of PBO. Also, data on the susceptibility to newer insecticides that are being introduced for vector control uses such as chlorfenapyr, clothianidin and broflanilide might have been an interesting addition. Response to reviewer 1: We appreciate the reviewer’s positive feedback and thoughtful suggestions. While our study focused on phenotypic resistance and target-site mutations, we acknowledge the importance of investigating specific metabolic resistance mechanisms, such as P450 gene expression. This limitation is now noted in the Discussion as a key area for future research. Regarding newer insecticides like chlorfenapyr and clothianidin and broflanilide our study focused on insecticides for which resistance markers were well-characterized at the time, to examine how phenotypic resistance and known genetic markers are distributed across species and ecological zones. These markers are increasingly used to inform insecticide deployment and resistance management strategies. We also recognize the importance of evaluating susceptibility to these newer compounds, and this has been highlighted as a priority in our future research directions. Response to reviewer 2: Reviewer #2: This study is about mosquito diversity and the distribution of resistance mechanisms among malaria vectors in three ecological areas in Côte d’Ivoire. The overall manuscript was very well written in easy English, with good results and important recommendations. I only have minor reviews which if addressed could help the readers to better understand the study. Minor reviews: 67 Please rephrase this sentence to make clearer when PBO was conducted Response 1: We thank the reviewer for this helpful observation. The sentence has been revised in the Abstract section and can be found at lines 66- 68 of the revised manuscript. 69-70 ‘target site mechanisms (Kdr L1014F and Ace-1R G119S) determined using PCR’ is there a ‘were’ that is missing? Response 2: We appreciate the reviewer’s attention to clarity. The sentence has been revised, and the updated version appears in the Abstract at line 71. 75 please delete ‘collected’ Response 3: We thank the reviewer for this suggestion. The word “collected” has been removed, as recommended in the line 76. 76-77 ‘in the savannah area (97-100% of collected mosquitoes)’ and in all the result part of the background please change the range to the mean of the proportion with the confidence interval (CI). For example ‘in the savannah area (97.9%, 95% CI [96.2-99.7]) or simply rephrase Response 4: We have replaced the percentage ranges with mean values and 95% confidence intervals in the Abstract and can be found at line 77-83. 96-97 please add some references about the seven species Response 5: Thank you to the reviewer. A supporting reference has been added at line 102 and in the References section (lines 380-381). 99 Please write some key findings of these authors in the text Response 6: Thank you. Key findings from the cited studies have been added to contextualize species variation and distribution at lines 99-102. 108 the introduction is well written however it lacks some related literature that had already shown by their results the importance of addressing insecticides resistances patterns according to species level in Côte d’Ivoire and other country of Africa. Please add some of them. It is not clear what the authors mean by ‘adequately’, please be more precise Response 7: We thank the reviewer for this valuable suggestion. Relevant literature highlighting the importance of assessing insecticide resistance patterns at the species level in Côte d’Ivoire has now been added at lines 109-112. We have also clarified the intended meaning of “adequately” to better reflect the novelty of our study at lines 112-115. 109-110 add some references from the country of study Response 8: We thank the reviewer for this helpful suggestion. References from studies conducted in Côte d’Ivoire have now been added to strengthen this statement (line 117) 100, 122, 167 italic for malaria vector name Anopheles, please check throughout the paper Response 9: Thank you for the observation. All malaria vector names, including Anopheles species have been i Attachments Attachment Submitted filename: Response to Reviewers_PONE-D-24-56516.docx https://doi.org/10.1371/journal.pone.0332497.r002
2 Sep 2025 Decision Letter - Adekunle Bakare, Editor Insecticide resistance and species diversity in Anopheles gambiae s.l. in Côte d’Ivoire PONE-D-24-56516R1 Dear Dr. Wolie, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. For questions related to billing, please contact billing support . 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, Adekunle Akeem Bakare, Ph.D. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0332497.r003
Formally Accepted
Acceptance Letter - Adekunle Bakare, Editor PONE-D-24-56516R1 PLOS ONE Dear Dr. Wolie, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset You will receive further instructions from the production team, including instructions on how to review your proof when it is ready. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few days to review your paper and let you know the next and final steps. Lastly, 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. You will receive an invoice from PLOS for your publication fee after your manuscript has reached the completed accept phase. If you receive an email requesting payment before acceptance or for any other service, this may be a phishing scheme. Learn how to identify phishing emails and protect your accounts at https://explore.plos.org/phishing. If we can help with anything else, please email us at customercare@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 Adekunle Akeem Bakare Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0332497.r004

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