The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo

Rodney N. Nagoshi; Djima Koffi; Komi Agboka; Anani Kossi Mawuko Adjevi; Robert L. Meagher; Georg Goergen

doi:10.1371/journal.pone.0253528

Peer Review History

Original SubmissionMarch 29, 2021
6 May 2021 Decision Letter - Ramzi Mansour, Editor PONE-D-21-10287 The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. PLOS ONE Dear Dr. Nagoshi, 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 15 June 2021. 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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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: No ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: No ****** 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: Nagoshi et al. analyzed marker sequences (mt-CO1 and TPI) from the samples collected both from rice and corn fields in the fall amryworm and concluded that rice strains do not exist or rarely exist in West Africa. I believe that their argument is supported by their result. However, I have the following concerns. 1. As the authors already showed in their previous papers, the vast majority of fall armyworms in Africa are hybrids between corn and rice strains. A genomic analysis does show evidence that invasive populations are a mixture of corn and rice strains (https://onlinelibrary.wiley.com/doi/full/10.1111/1755-0998.13219). Thus, what we know now is that fall armyworms from corn fiend in invasive populations are hybrids, not corn strain. Thus, if similar sequences were observed between samples from corn and rice fields, it is fair to say that the samples from rice fields are hybrids, not corn strain. But throughout the whole manuscript, it appears that they assume that African fall armyworms from corn fields are corn strains. But this assumption seems to be incorrect. 2. In the same context, they have to make it clear what they mean corn strain and rice strain. Are they a taxonomic group? Or just grouping according to the sampling site? 3. Line 51-52. Independent segregation between CO1 and TPI is not true. A half of nuclear genomes is from mother. Thus, 50% of genomes co-segregate with mt-CO1. 4. Table 1, to me, larvae collected from plants by hand could be very different from adults collected by pheromone trap. The adults collected near rice field might have grown up in corn field. They need to show that these adults were grown up on rice field in order not to say that corn strains accidentally arrived near rice fields. 5. L229-L230. They have to provide a reference. And it is really unclear because, at L23-L25, they say that fall armyworms are not a major risk for rice. 6. L347. Indeed, they analyzed a very low number of samples from rice field. Thus, all statistical analyses could not be performed properly because of insufficient statistical power. I do understand that it could have been difficult to collect insects from rice field. And this fact itself might be sufficient to say that there is no established population on rice field. Reviewer #2: In this paper, authors described “The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo.” Authors have field detection and lab hybrid work upon FAW. Data providing was sufficiently enough, while the inconsistent or conflict recognition on R-strain or C-strain confuse their result and the following discussion. Actually, authors have a conflict result upon the FAW recognition of R-strain and C-strain between the mitochondrial and nuclear DNA markers, i.e. intermediate types of COI-CS/TpiC and COI-RS/TpiC. They also mentioned and suggested that the COI gene, is not an accurate indicator of strain identity for the African fall armyworm populations. Therefore, how do they elucidate definitely the R-strain is rare or absent in Africa. Several molecular evidences have shown that R- and C-strains with undistinguishable morphology are generally sympatric in the field, implying the possibility of genetic exchange between the two evolutionary groups. Moreover, molecular evidences also revealed that more than two genetically distinct clusters existed in FAW; therefore, distinguishing the C-strain from Rice-form based on their host plant and genetic markers is unlikely necessary. Authors also shown African FAW do not display strain-specific mating patterns. It is undoubtedly important work to know the population structure upon African FAW, but it documented unsuitable based on R- and C-strain. ****** 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. 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Attachments Attachment Submitted filename: suggestion.pdf https://doi.org/10.1371/journal.pone.0253528.r001
Revision 1
15 May 2021 Author Response Response to Journal. < 3. We note that Figure 1 in your submission contains map images which may be copyrighted.> Added to Figure legend that the map image is QGIS open source. Response to reviewers. We thank the reviewers for their comments and have tried to address all the concerns. Extensive changes were made to the introduction and discussion to provide a clearer explanation of the strains and markers, as well as the rationale for the experiments. Minor alterations were made to Figures 5 and 6 that did not change the conclusions made from the data. Reviewer’s comments are bracketed (< >). <1. As the authors already showed in their previous papers, the vast majority of fall armyworms in Africa are hybrids between corn and rice strains… Thus, what we know now is that fall armyworms from corn field in invasive populations are hybrids, not corn strain.> The assertion that the Africa fall armyworm are hybrids is an explanation for their unusual configuration of genetic markers. However, there is no indication that they are hybrid in their strain identity (in other words as far as we can tell the African fall armyworm are behaving like the C-strain in their plant host use). A paragraph was added to the introduction (lines 71-79) to explain this distinction. <But throughout the whole manuscript, it appears that they assume that African fall armyworms from corn fields are corn strains. But this assumption seems to be incorrect.> We have gone through the manuscript to remove such assumptions. For example, the term C-strain or corn strain are not used in the Results section. Instead, the specimens are described by their COI or Tpi haplotype. We also now provide in the discussion an explanation of why we believe the African fall armyworms can be considered C-strain (lines 375-385) <2. In the same context, they have to make it clear what they mean corn strain and rice strain. Are they a taxonomic group? Or just grouping according to the sampling site?> We added a paragraph to the introduction describing the difficulties in categorizing what the strains represent (lines 47-55). In addition, we note that lines 56-70 in the introduction describe method and rationale for how we defined strains in this paper. <3. Line 51-52. Independent segregation between CO1 and TPI is not true. A half of nuclear genomes is from mother. Thus, 50% of genomes co-segregate with mt-CO1.> We corrected this error in lines 60-62. <4. Table 1, to me, larvae collected from plants by hand could be very different from adults collected by pheromone trap. The adults collected near rice field might have grown up in corn field. They need to show that these adults were grown up on rice field in order not to say that corn strains accidentally arrived near rice fields.> As noted in lines 184-190, the larval collections are treated differently from pheromone trap collections when appropriate. We discuss at some length the possibility that the rice pheromone trap specimens come from other hosts (lines 360-372) and have tempered our conclusions with that in mind. We added references to examples where pheromone traps in the Western Hemisphere have successfully collected populations with strain identities that correspond with the local host plants (lines 354-355). <5. L229-L230. They have to provide a reference. And it is really unclear because, at L23-L25, they say that fall armyworms are not a major risk for rice.> We don’t believe a reference here is unnecessary since in this section we describe in detail fall armyworm infestations of rice in South America (references are in 243-247). We also removed lines 23-25 from the revised abstract. <6. L347. Indeed, they analyzed a very low number of samples from rice field. Thus, all statistical analyses could not be performed properly because of insufficient statistical power. I do understand that it could have been difficult to collect insects from rice field. And this fact itself might be sufficient to say that there is no established population on rice field.> We do not understand this criticism. If we look at Figure 5 for example the sample size for rice ranged from 45 to 109, which is pretty high for this type of study and similar in range to the sampling from corn. Reviewer #2: In this paper, authors described “The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo.” Authors have field detection and lab hybrid work upon FAW. Data providing was sufficiently enough, while the inconsistent or conflict recognition on R-strain or C-strain confuse their result and the following discussion.> We made major revisions to the introduction and discussion to address this criticism. <Actually, authors have a conflict result upon the FAW recognition of R-strain and C-strain between the mitochondrial and nuclear DNA markers, i.e. intermediate types of COI-CS/TpiC and COI-RS/TpiC. They also mentioned and suggested that the COI gene, is not an accurate indicator of strain identity for the African fall armyworm populations. Therefore, how do they elucidate definitely the R-strain is rare or absent in Africa.> The conclusion that the R-strain is rare is based on the frequency of the TpiR marker and lack of fall armyworm in host plants and habitats preferred by the R-strain. In response to the reviewer, we expanded the relevant section of the Discussion on this point (lines 349-374). We also describe why we believe that the Tpi marker may still be relevant for strain identification in the introduction (lines 71-79) and Discussion (lines 375-399). <Several molecular evidences have shown that R- and C-strains with undistinguishable morphology are generally sympatric in the field, implying the possibility of genetic exchange between the two evolutionary groups. Moreover, molecular evidences also revealed that more than two genetically distinct clusters existed in FAW; therefore, distinguishing the C-strain from Rice-form based on their host plant and genetic markers is unlikely necessary. > Not sure what other genetic clusters are being referred to here, but we believe the strains are of particular importance because they differentiate fall armyworm based on plant host use. This has important implication when determining what plant types are at risk. We added a section to better explain this point of view to the introduction (lines 71-86). We also added additional material to the discussion describing our interpretation of the fall armyworm strains found in Africa (lines 375-399). <Authors also shown African FAW do not display strain-specific mating patterns. It is undoubtedly important work to know the population structure upon African FAW, but it documented unsuitable based on R- and C-strain.> We disagree. At this time the strain markers are the only ones that have been demonstrated (in the Americas) to distinguish fall armyworm for their host plant preference, which has obvious relevance to identifying what crops are at risk. As detailed above, we have made extensive revisions to the introduction and discussion to explain our perspective. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0253528.r002
27 May 2021 Decision Letter - Ramzi Mansour, Editor PONE-D-21-10287R1 The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. PLOS ONE Dear Dr. Nagoshi, 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 Jul 11 2021 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. Please include the following items when submitting your revised manuscript: 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'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Ramzi Mansour Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] 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 #2: (No Response) ******** 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 #2: Partly ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: N/A ****** 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 #2: Yes ****** 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 #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 #2: Authors could have an outstanding elucidation for African FAW structure, while the R-strain and C-strain is now not a natural recognition. As the authors showed either in the previous version or this version, L71-79, that hybridization between Corn-strain and Rice-strain has been occurred and showed disagreement between the mtCOI and nrTpi strain haplotypes. Authors also know that there have several publishings documented that more than two genetic lineages could be found in FAW. It is already unmeaningful to distinguish R- from C-strains for FAW as I have suggested in the previous version. It is undoubtedly important work to know the population structure upon African FAW, but the R- and C-strain documentation should be abandoned. ****** 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 #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. Attachments Attachment Submitted filename: suggestion for R1.pdf https://doi.org/10.1371/journal.pone.0253528.r003
Revision 2
29 May 2021 Author Response We do not agree with the reviewer’s comments. The primary objection of the reviewer is: “It is already unmeaningful to distinguish R- from C-strains for FAW as I have suggested in the previous version”. We strongly disagree with that statement and believe the reviewer has not taken into consideration the following points. First, all previous work on FAW population genetics in Africa have been done on specimens collected from corn or less frequently sorghum. These are host plants associated with the C-strain. Very little is known about whether FAW is associated with R-strain hosts in Africa and if so, what the strain composition of these might be. I want to emphasize that point, the characterization of FAW associated with R-strain host plants in Africa has not been done previously and without that analysis one cannot assume the absence of the R-strain in Africa. To do so, as appears to be what is being suggested by the reviewer, is not good science. This point is explicitly made several times in the paper (see for example lines 8-16 in the abstract, lines 85-89 in the introduction, and lines 353-354 in the Discussion). It is even alluded to in the lines noted by the reviewer (L71-79) where we state “Because virtually all the Eastern Hemisphere specimens tested to date were collected from the C-strain associated hosts corn and sorghum,…” (L74-76). This is the issue being addressed by this manuscript. This is the first, and so far only, attempt to systematically collect and genetically analyze FAW in Africa from R-strain hosts. As such we believe it is a critically important paper for assessing the status of the two strains in Africa. To make this point explicitly clear lines 79-81 and 88-89 were added to the Introduction. Second, the assertion by the reviewer that the strains are no longer relevant in Africa and that “the R- and C-strain documentation should be abandoned” is at best premature and most likely wrong. The defining characteristic of the strains is host plant preference. The defining characteristic of the C-strain is that it primarily infests corn and sorghum fields, only occasionally rice, and very rarely pasture grasses. This manuscript demonstrates that the Africa FAW is showing a similar preference pattern. It is found in corn, is ambiguous in rice (trap captures but little evidence of larval infestation), and virtually absent in pasture grasses. So even if there was an ancestral hybridization event between the strains, the Africa FAW population is effectively still behaving like the C-strain. What has changed is that COI is no longer an accurate strain marker. This point is explicitly made in Lines 74-78 in the Introduction and 384-387 in the Discussion. We also provided an explanation for how this might have occurred where an early hybridization event between strains disassociated the COI marker but still maintained a C-strain identity/behavior (lines 377-401). Third, the reviewer does not consider the fact that the R-strain does exist in the Western Hemisphere and so could enter Africa at any time. So even if the current African FAW is a hybrid, secondary introductions of FAW to Africa could return both strains into the continent with potential economic consequences. Therefore, continued surveillance of Africa populations with the strain markers is still relevant and important as is noted in lines 421-424. The reviewer also stated: “Authors also know that there have several publishings (sic) documented that more than two genetic lineages could be found in FAW.” We believe these lineages are irrelevant to this paper as the lineages are not associated with host preference. This paper is about whether the two FAW lineages associated with different host plant preferences in the Western Hemisphere are present in Africa. In summary, we believe the reviewer’s objections are not reasonable and stem from assumptions that are premature and probably incorrect. This manuscript represents the first systematic attempt to find and genetically characterize Africa FAW in the R-strain hosts of rice and pasture grasses. This information is critical to the assessment as to whether the fall armyworm population likely to threaten rice, millet, and pasture grasses is present Africa. Attachments Attachment Submitted filename: Response to Reviewers2.docx https://doi.org/10.1371/journal.pone.0253528.r004
8 Jun 2021 Decision Letter - Ramzi Mansour, Editor The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. PONE-D-21-10287R2 Dear Dr. Nagoshi, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication (BUT, please see and apply ADDITIONAL EDITOR COMMENTS below) 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, Ramzi Mansour Academic Editor PLOS ONE Additional Editor Comments: The following revisions should be made by the authors on the PROOFS of their accepted article: L23 (Abstract): please replace "Ghana-Togo region" with "Ghana-Togo area" L27 (Introduction): please replace "(Spodoptera frugiperda) is" with "Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) is" L34: please replace "plant hosts" with "host plants" L54: please replace "and plant host" with "and host plant" L100 (Materials and methods): please replace "Fall armyworm was collected" with "Fall armyworm individuals were collected" L124: please leave one space after "6000" L124: please delete the " . " after "5 min" L130: 10 mM L145: please add a comma before "the first PCR" L185-186: the number of TpiH specimens were incorporated ?? something is wrong here, please correct (the numbers ?) L238 (Figure 3 caption): please replace "pheromone trap capture numbers" with "pheromone trap captures" L259: please replace "plant types" with "plant species" L263: please add "and" before "Murua" L298: please add the Authorship, Order and Family "(Boisduval) (Lepidoptera: Noctuidae)" just after "Spodoptera littoralis" as this species is mentioned for the first time here L299: the common name abbreviation "FAW" is mentioned for the first time in the paper with no previous definition; for consistency with what is written throughout the text, I'd suggest replacing "FAW" with "fall armyworm" L301: Larvae were also L327: please leave one space before "(Fig 6)" L352 (Discussion): please replace "affected regions" with "affected areas" L358: please add a comma after "efforts" L364: please add a comma after "and Togo" L365-366: please replace "in this region" with "in this western African area" L368: please change to ", that fall armyworms collected in the" L373-373: please change to "Regardless of origin, fall armyworms found in rice traps were" L419: please replace "Africa populations" with "African fall armyworm populations" L420: associated host plants Reviewers' comments: https://doi.org/10.1371/journal.pone.0253528.r005
Formally Accepted
11 Jun 2021 Acceptance Letter - Ramzi Mansour, Editor PONE-D-21-10287R2 The fall armyworm strain associated with most rice, millet, and pasture infestations in the Western Hemisphere is rare or absent in Ghana and Togo. Dear Dr. Nagoshi: 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. Ramzi Mansour Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0253528.r006

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