Population genetic structure and historical demography of the population of forest elephants in Côte d’Ivoire

Jean-Louis Kouakou; Sery Gonedelé-Bi

doi:10.1371/journal.pone.0300468

Peer Review History

Original SubmissionJune 23, 2023
26 Dec 2023 Decision Letter - Tunira Bhadauria, Editor PONE-D-23-19598Population genetic structure and historical demography of the population of forest elephants in Côte d’IvoirePLOS ONE Dear Dr. Gonedelé Bi, 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 Feb 09 2024 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. 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If you are unable to adhere to our open data policy, please kindly revise your statement to explain your reasoning and we will seek the editor's input on an exemption. Please be assured that, once you have provided your new statement, the assessment of your exemption will not hold up the peer review process. [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: The manuscript analyzes 101 sequences from three populations of Loxodonta cyclotis in Côte d’Ivoire (Africa): Bossématié, Dassioko and Port-Gauthier classified forests. The authors analyzed a 600pb fragment from the hypervariable I section of the mitochondrial control region. Based on this genetic marker they evaluated the genetic diversity, the population genetic structure, and population demographic history of forest elephant in Côte d’Ivoire. The authors observed low gene flow between the Bossématié population and the other populations, likely resulting from geographical isolation caused by fragmentation. Additionally, they found that the size of Loxodonta cyclotis populations in Côte d’Ivoire remained constant over time. This manuscript represents a high contribution towards the Loxodonta cyclotis genetic population and conservation. However, I have noticed some crucial issues that need to be addressed: 1) The text requires reorganization. For example, the methodology should clearly state how the sequences were curated leaving only 101 sequences and avoid re-presenting information already presented in the result section in the discussion section. 2) The utilization of a highly variable sequence to infer species diversity and population historical demography represents a weakness in this study. The authors should, at the very least, acknowledge their awareness of this limitation. In comparison, all other studies used for reference employed at least two genetic markers, including less variable regions. If the authors followed a similar approach, they should emphasize it in the manuscript. 3) I noticed that the supplementary material mentioned in line 326 is missing, as well as the GenBank accession numbers of the sequences they obtained. 4) Figure 4 and line 383: Based on this graphic, it is not possible to infer a correlation between genetic distance and geographical distance. While it is conceivable that this genetic marker should exhibit an isolation by distance pattern, the current graphic does not demonstrate such a relationship. 5) Phylogenetic relationships cannot be reliably inferred using only one variable genetic marker. I recommend refraining from drawing such conclusions throughout the text. As for Figure 5, it is evident that these individuals possess distinct haplotypes in comparison to other works, while also sharing similar haplotypes among themselves. However, no definitive conclusions about their phylogenetic relationships can be drawn from this data alone. Reviewer #2: This is well-written manuscript and based on impressive empirical evidence and makes an original contribution. The abstract is adequately addressed. The Introduction is adequate. The literature review is concise updated covering the main relevant concept and empirical studies on different approaches on this field. In material methods sample collection, DNA extraction, PCR sequencing and data analysis is properly maintained as per this research work demand . The results are clearly presented with proper statistical methods and adequately addressed. The authors develop a unique theoretical framework and highlighted originality much more. The study may be assist to maintain elephant populations of Dassioko, Port Gauthier, Zoo of Abidjan and Bossematie . Therefore , the manuscript can be considered for the publication. ****** 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: Yes: Juliana Cordeiro Reviewer #2: Yes: Dr. Dhananjay Singh ******** [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.0300468.r001
Revision 1
29 Jan 2024 Author Response Reviewer #1: This manuscript represents a high contribution towards the Loxodonta cyclotis genetic population and conservation. However, I have noticed some crucial issues that need to be addressed: 1) The text requires reorganization. For example, the methodology should clearly state how the sequences were curated leaving only 101 sequences and avoid re-presenting information already presented in the result section in the discussion section. 1) Answer Of the 137 samples with a positive simplex PCR, 80.30 % (110 out of 137) were successfully sequenced. As part of this study, 47, 41 and 13 good quality sequences of the mitochondrial DNA control region (CSB1) obtained from dung samples respectively collected in the Bossématié (FCB), Dassioko (FCD) and Port-Gauthier (FCPG) Forest Reserves. These 130 sequences were taken into account for different analyses. 2) The utilization of a highly variable sequence to infer species diversity and population historical demography represents a weakness in this study. The authors should, at the very least, acknowledge their awareness of this limitation. In comparison, all other studies used for reference employed at least two genetic markers, including less variable regions. If the authors followed a similar approach, they should emphasize it in the manuscript. 2) Answer The genetic profile established in this study is based on mitochondrial DNA (mtDNA) control region, which is only transmitted maternally. This non-coding genetic marker commonly used in conservation genetic studies to examine genetic structure at the population level because it is considered to be the most rapidly evolving region of the mitochondrial genome (Baker and Marshall 1997; Ruokonen 2002). This locus is broadly considered to be suitable for examining intraspecific relationships among closely related groups of individuals (Sinclair and Pe´rez-Losada 2005). However, the use of mtDNA control region presents some limitations resulting from the fact that the analysis of mtDNA corresponds to the study of a single locus. This means that the total dependence on mtDNA as a marker in the study of the natural history of populations will give only a small part of that history (Zhang & Hewitt 2003). Indeed, the high evolutionary rate that has made the control region an attractive marker for biologists may be masking the true relationships between populations due to high haplotype diversity as well as homoplasy. Hence, the use of an alternative marker with a slower evolutionary rate may be more suitable than the control region to reveal the population structure of forest elephant. 3) I noticed that the supplementary material mentioned in line 326 is missing, as well as the GenBank accession numbers of the sequences they obtained. 3) Answer The GenBank accession numbers of the sequences obtained have been included as suggested by the reviewer. The additional material mentioned is available from line 521 to 523. Data Availability Statement: Sequence data are available in GenBank https://www.ncbi.nlm.nih.gov/nuccore/MZ485910.1,MZ485851.1,MZ485850.1, MZ485849.1,MZ485848.1,MZ485847.1,MZ485846.1,MZ485845.1,MZ485844.1,MZ485843.1,MZ485842.1,MZ485841.1,MZ485840.1,MZ485839.1,MZ485838.1,MZ485834.1,MZ485833.1,KJ557424.1,MZ485831.1,MZ485830.1,MZ485829.1,MZ485828.1,MZ485827.1,MZ485826.1,MZ485825.1,MZ485824.1,MZ485823.1,MZ485822.1,MZ485821.1,MZ485820.1,MZ485819.1,MZ485818.1,MZ485817.1,MZ485816.1,MZ485815.1,MZ485814.1,MZ485813.1,MZ485812.1,MZ485811.1,MZ485810.1,MZ485809.1,MZ485852.1,MZ485909.1,MZ485903.1,MZ485900.1,MZ485899.1,MZ485898.1,MZ485896.1,MZ485895.1,MZ485894.1,MZ485892.1,MZ485891.1,MZ485890.1,MZ485889.1,MZ485881.1,MZ485880.1,MZ485879.1,MZ485878.1,MZ485877.1,MZ485871.1,MZ485870.1,MZ485869.1,MZ485866.1,MZ485865.1,MZ485864.1,MZ485863.1,MZ485862.1,MZ485861.1,MZ485859.1,MZ485858.1,MZ485856.1,JQ438209.1,MZ485905.1,MZ485904.1,MZ485887.1,MZ485886.1,MZ485885.1,MZ485882.1,MZ485873.1,MZ485872.1,MZ485836.1,MZ485832.1,MZ485888.1,MZ485883.1,MZ485908.1,MZ485907.1,MZ485906.1,MZ485902.1,MZ485876.1,MZ485874.1,MZ485860.1,MZ485837.1,MZ485835.1,JQ438745.1,MZ485893.1,MZ485884.1,MZ485901.1,MZ485897.1,MZ485868.1,MZ485867.1 List the number of samples collected in the Genbank database used in this study (Tables 3). Table 3 Accession numbers for samples included in this study. Species Sample origin Accession number Citation Loxodonta cyclotis Côte d’Ivoire KJ557424.1 [71] Gabon KJ557423 [71] Sierra Léone JN673264 [70] République centrafricaine JN673263 [70] Loxodonta africana Savanne 1 AB443879.1 [80] Savanne 2 NC_000934.1 [81] Savanne 3 DQ316069.1 [82] Elephas maximus Asie 1 DQ316068 [73] Asie 2 NC_005129 [73] Asie 3 EF588275 [64] Mammuthus primigenius Mammouth EU155210 [83] 4) Figure 4 and line 383: Based on this graphic, it is not possible to infer a correlation between genetic distance and geographical distance. While it is conceivable that this genetic marker should exhibit an isolation by distance pattern, the current graphic does not demonstrate such a relationship. 4) Answer The Mantel test shows a strong and positive but not significant correlation, between genetic and geographical distances (Monte Carlo randomisation test, Rxy = 0.97; P = 0.37). Which does not suggest isolation by distance (IBD). 5) Phylogenetic relationships cannot be reliably inferred using only one variable genetic marker. I recommend refraining from drawing such conclusions throughout the text. As for Figure 5, it is evident that these individuals possess distinct haplotypes in comparison to other works, while also sharing similar haplotypes among themselves. However, no definitive conclusions about their phylogenetic relationships can be drawn from this data alone. 5) Answer Figure 5 illustrates the relationships between the mtDNA control region sequences generated during this study and those of forest elephant (Loxodonta cyclotis), savanna elephant (L. africana), Mammuthus primigenius, and Elephas maximus retrieved from the National Center for Biotechnology Information (NCBI) database. The phylogenetic analysis of the subpopulations of the Bossématié, Dassioko, and Port Gauthier CFs shows that they appear monophyletic, with heterogeneous structuring (genetic variation) in a clade with the forest elephants selected in the NCBI da-tabase. Based on the sequence analysed, the phylogenetic study showed that forest elephants and savannah elephants form two different clades. This analysis detected that Asian elephants (E. maximus) and the Mammuthus primigenius clade form a clade in their own right, which differs from those of forest elephants and savannah elephants (Fig 5). We are aware that Phylogenetic relationships cannot be reliably inferred using only one variable genetic marker. Particularly data from nonrecombining mitochondrial DNA (mtDNA), has important limitations that ares now widely recognized. Indeed, a mtDNA tree may be different from the population or species tree due to the effects of natural selection (see, for example, Weinreich & Rand 2000 and Bazin et al. 2006), introgression (Chan & Levin 2005; Melo-Ferreira et al. 2005) or the wide stochastic variance that characterizes a sample of gene trees collected from a set of populations or species (Hey & Machado 2003). Hence, no definitive conclusions about their phylogenetic relationships can be drawn from the obtained data alone. Reviewer #2: This is well-written manuscript and based on impressive empirical evidence and makes an original contribution. The abstract is adequately addressed. The Introduction is adequate. The literature review is concise updated covering the main relevant concept and empirical studies on different approaches on this field. In material methods sample collection, DNA extraction, PCR sequencing and data analysis is properly maintained as per this research work demand. The results are clearly presented with proper statistical methods and adequately addressed. The authors develop a unique theoretical framework and highlighted originality much more. The study may be assist to maintain elephant populations of Dassioko, Port Gauthier, Zoo of Abidjan and Bossematie. Therefore, the manuscript can be considered for the publication. Good Attachments Attachment Submitted filename: Responses to reviewers_gs_27janvier2024_2.docx https://doi.org/10.1371/journal.pone.0300468.r002
28 Feb 2024 Decision Letter - Tunira Bhadauria, Editor Population genetic structure and historical demography of the population of forest elephants in Côte d’Ivoire PONE-D-23-19598R1 Dear Dr. Bi 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, Tunira Bhadauria, Ph.D. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0300468.r003
Formally Accepted
4 Apr 2024 Acceptance Letter - Tunira Bhadauria, Editor PONE-D-23-19598R1 PLOS ONE Dear Dr. Gonedelé Bi, 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 If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks 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. 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 Dr. Tunira Bhadauria Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0300468.r004

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