Abstract

Concerns about the prospect of a global pandemic have been triggered many times during the last two decades. These have been realised through the current COVID-19 pandemic, due to a new coronavirus SARS-CoV2, which has impacted almost every country on Earth. Here, we show how considering the pandemic through the lenses of the evolutionary ecology of pathogens can help better understand the root causes and devise solutions to prevent the emergence of future pandemics. We call for better integration of these approaches into transdisciplinary research and invite scientists working on the evolutionary ecology of pathogens to contribute to a more "solution-oriented" agenda with practical applications, emulating similar movements in the field of economics in recent decades.


Authors

Roche, Benjamin;  Garchitorena, Andres;  Guegan, Jean-Francois;  Arnal, Audrey;  Roiz, David;  Morand, Serge;  Zambrana-Torrelio, Carlos;  Suzan, Gerardo;  Daszak, Peter

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  • pre-publication peer review (FINAL ROUND)
    Decision Letter
    2020/07/12

    Canberra, 12-Jul-2020

    Manuscript number: ELE-00701-2020.R1
    Title: Was the COVID-19 pandemic avoidable? A call for a “solution-based” approach in pathogen evolutionary ecology to prevent future outbreaks
    Author(s): Roche, Benjamin; Garchitorena, Andres; Guegan, Jean-Francois; Arnal, Audrey; Roiz, David; Morand, Serge; Zambrana-Torrelio, Carlos; Suzan, Gerardo; Daszak, Peter
    Type: Viewpoints
    Editor: Dr. Peter Thrall
    Manuscript received: 13-May-2020
    Manuscript accepted:

    Dear Dr. Roche,

    I am delighted to say that your manuscript is now accepted for publication in Ecology Letters. Our first Viewpoint!

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    Editor: Thrall, Peter
    Editors Comments for the Author(s):
    (There are no comments.)


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    Author Response
    2020/07/09

    Montpellier, Mexico City, New York City, Bangkok, July 10th 2020

    Resubmission of MS #ELE-00533-2020: Was COVID-19 pandemic avoidable? A call for a “solution-based” approach in evolutionary ecology of pathogens for preventing future outbreaks

    Dear Pr Thrall,

    Thank you for giving us the opportunity to submit a revised draft of our manuscript titled “Was COVID-19 pandemic avoidable? A call for a “solution-based” approach in evolutionary ecology of pathogens for preventing future outbreaks” to Ecology Letters.

    We appreciate the effort that you have dedicated to providing thoughtful comments and constructive suggestions, which help to improve the quality of the manuscript. We have integrated all your editing suggestions as well as considered the suggestions you made with the aim of sharpening more our perspective.

    In brief, we have changed quite substantially the last part of our viewpoint to highlight two important take-home messages: (i) Evolutionary ecology of pathogens are not considered enough by decision-makers to prevent pandemics emergence, (ii) our scientific community has to make to produce more “solution-oriented” research, in order that the knowledge we produce can be concretely used by the relevant authorities.

    Benjamin Roche
    On the behalf of the co-authors



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  • pre-publication peer review (ROUND 2)
    Decision Letter
    2020/07/08

    Dr. Benjamin Roche IRD/UPMC 32, rue henri varagnat
    Bondy
    Ile de France
    France
    93143

    Canberra, 08-Jul-2020

    Dear Dr. Roche,


    UPDATE:
    The coronavirus epidemic is impacting ecologists around the globe, with fieldwork, office work, and lab work all affected as people work from home and self-isolate. In addition, in some countries, schools are shut, which means many of us will be looking after children at home. We appreciate that this disruption can impact all aspects of work and home life. For that reason, we are pleased to provide extensions to manuscript revisions. If you miss a deadline to resubmit a manuscript, please do not worry – we will reopen the submission pipeline when you are ready to resubmit. Stay well. Best wishes, from all of us at Ecology Letters


    Manuscript number: ELE-00701-2020 Title: Was COVID-19 pandemic avoidable? A call for a “solution-based” approach in evolutionary ecology of pathogens for preventing future outbreaks Author(s): Roche, Benjamin; Garchitorena, Andres; Guegan, Jean-Francois; Arnal, Audrey; Roiz, David; Morand, Serge; Zambrana-Torrelio, Carlos; Suzan, Gerardo; Daszak, Peter

    I've gone through the editorial again (I did not send it to a handling editor this time but attach some comments on the doc). I think it is definitely improved. I'd like you to have one more go at it with the aim of sharpening a bit more your perspective. Perhaps consider things like: Where do you see opposition to what you are suggesting? Are there alternative views? Are there any challenges or concerns with implementing these frameworks?

    In general, I'm hoping that Viewpoints editorials will generate broader discussion and debate on topics where ecology/evolution has something to say but where other domains (e.g. social, policy, environmental, economic) would have an interest.

    Yours sincerely,

    Dr Peter Thrall
    Senior Editor
    Ecology Letters


    Referees' comments to the author(s):


    Editor's comments to the author(s):

    Editor
    Editors Comments for the Author(s):
    (There are no comments.)


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    Author Response
    2020/06/25

    Resubmission of MS #ELE-00533-2020: Was COVID-19 pandemic avoidable? A call for a “solution-based” approach in evolutionary ecology of pathogens for preventing future outbreaks

    Montpellier, June 23rd 2020

    Dear Pr Thrall,

    Thank you for giving us the opportunity to submit a revised draft of our manuscript titled “Was COVID-19 pandemic avoidable? A call for a “solution-based” approach in evolutionary ecology of pathogens for preventing future outbreaks” to Ecology Letters.

    We appreciate the effort that you and the associated editor have dedicated to providing thoughtful comments and constructive suggestions, which help to improve the quality of the manuscript. We have integrated all your editing suggestions and replied to each point raised by the editor who reviewed our paper. In short, we provided a clearer guidance on how developing more “solution-based” research in evolutionary ecology of pathogens. We have also highlighted some research that have been already applied this kind of “solution-based” research. You will find below a point-by-point response to each comment.

    Benjamin Roche
    On the behalf of the co-authors

    Editor’s comment:
    The Viewpoints manuscript by Roche et al argues that “the many scientists working on evolutionary ecology of pathogens” should “shift from purely academic research towards operational research to devise practical applications…” to the covid-19 pandemic. This is the primary statement in the abstract and in the closing paragraph. Unfortunately, this position is undermined by three essential weaknesses.

    First, the “operational research to devise practical applications” is not defined. What should evolutionary ecologists working on pathogens start working on, and what basic research should they abandon to accomplish such a shift?

    Answer:
    We agree that this point was missing clarity. First, the call to shift between fundamental and operational research was definitely not the best one. Instead, we integrate now more subtilty and call for a stronger integration of “solution-based” research, which is reflecting more precisely what we had in mind. This has been clarified throughout the manuscript.

    Editor’s comment:
    Second, assuming that pathogen ecologists shifted wholesale from basic to applied research, the authors provide no guidance on what the applied research should look like and how it would prevent the next pandemic.

    Answer:
    We also agree with this comment and we have highlighted some research avenues towards this goal (lines 110-119):

    Understanding the underlying drivers of pathogen spillover and the role of biodiversity in pathogen transmission can help devise proactive ecological interventions to prevent and reduce spillover events. Indeed, ecosystem management and other strategies to protect species diversity, including restoration, rewilding and the management of wildlife reserves, halt habitat loss, population declines and illegal wildlife trade, can be a lever to prevent and mitigate pathogen emergence and transmission. In addition, increasing rates of emergence from domestic animals can be attributed to the demographic explosion and genetic homogeneity derived from intensive farming systems, where they can act as amplifiers and edge-hosts of novel pathogens. Increasing host diversity within farming systems can moderate their role in the emergence of new pathogens, as has been shown for plant pathogens13.

    Lines 134-142:

    We know that this human-animal interface can potentially impact pathogen adaptation to human populations. So far, most of the medical research focused on this topic consist in finding genetic markers demonstrating that an adaptation has taken place and would yield an efficient human-human transmission16. However, fundamental research accumulated on this topic in evolutionary ecology can bring important insights by identifying how such adaptation to a new host can be promoted17. Such studies could therefore provide practical knowledge for pandemic risk management if they become rooted in real-world data (e.g., through considering contact data between human and animal species) and/or on experimental models that can mimic closely human/animal contact processes.

    Editor’s comment:
    Third, the invitation to make this shift “towards operational research more connected to the field” is not supported by any of the material presented in the remainder of the Viewpoint. The bulk of the essay describes potential environmental drivers of pathogen spillover or emergence and human behavioural factors such as encroachment into natural systems, animal husbandry, and global travel. But this is entirely unrelated to the research that scientists working on evolutionary ecology of pathogens currently do or what the authors think they should do.

    Answer:

    We plaid guilty for a lack of clarity. We have now added a paragraph showing examples of “solution-based” research based on a previous fundamental scientific body (lines 144-153):

    While we now have a substantial understanding about the ecological and evolutionary drivers of pathogen spillover, there is a critical evidence gap on which ecological interventions can effectively reduce human disease burdens and pandemic risk. Examples exist, such as pilots on prawn farming to control schistosomiasis via a reduction of the snail intermediate host, or using landscape management to modify bat distribution and reduce risk to bat-borne pathogens. Nevertheless, these remain scarce 18,19. In this sense, one of the greatest opportunities in disease ecology lies in integrating pathogen data collection and evaluation methods (e.g. observational, quasi-experimental) with the myriad of ecosystem management and conservation efforts happening around the world.

    We have also rewritten the conclusion along these lines (lines 199-215):

    We call for an urgent consideration of ecological and evolutionary approaches to understand and model pandemics in a changing world in order to prevent them. Once again, we argue for transdisciplinary research conducted under the Ecohealth, OneHealth and Planetary Health frameworks. These initiatives can help us understand the connection between pathogen spread within human populations, inter-specific pathogen transmission within animal communities, and how this may lead to human adaptation. Practical insights into how landscape-use, biodiversity conservation and other ecosystem management processes affect disease emergence are also needed.

    We also call on scientists working on the evolutionary ecology of pathogens to integrate “solution-oriented“ research, more connected to the field, in order to devise solutions and practical applications of scientific results, emulating similar movements than in the field of economics and other social sciences in the recent decade 22. Biodiversity conservation, landscape management and theoretical evolution (among others) could all be “solution-based” research if applied to relevant pathogen models. Such “solution-based” research agenda could improve our capacity to avoid the next COVID-19-like catastrophe.

    We hope that we have convinced the editor of the added value of our call.



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  • pre-publication peer review (ROUND 1)
    Decision Letter
    2020/05/26

    Dr. Benjamin Roche
    IRD/UPMC
    32, rue henri varagnat
    Bondy
    Ile de France
    France
    93143

    Canberra, 26-May-2020

    Dear Dr. Roche,


    UPDATE:
    The coronavirus epidemic is impacting ecologists around the globe, with fieldwork, office work, and lab work all affected as people work from home and self-isolate. In addition, in some countries, schools are shut, which means many of us will be looking after children at home. We appreciate that this disruption can impact all aspects of work and home life. For that reason, we are pleased to provide extensions to manuscript resubmissions. If you miss a deadline to resubmit a manuscript, please do not worry – we will reopen the submission pipeline when you are ready to resubmit. Stay well. Best wishes, from all of us at Ecology Letters.


    Manuscript number: ELE-00533-2020
    Title: Was COVID-19 pandemic avoidable? A call for operational research in evolutionary ecology of pathogens for preventing future outbreaks
    Author(s): Roche, Benjamin; Garchitorena, Andres; Guegan, Jean-Francois; Arnal, Audrey; Roiz, David; Morand, Serge; Zambrana-Torrelio, Carlos; Suzan, Gerardo; Daszak, Peter

    While we are still working through a process for how to handle submissions to Viewpoints, I have additionally asked one of the editorial board members to provide comments (these are provided below). I think that they raise some good points. I have also made some comments and suggestions directly on the manuscript itself (attached).

    Although based on the comments from the handling editor, I have decided to decline your manuscript for publication consideration in Ecology Letters, if you believe that you can fully address the points raised by the reviewers, then we would be prepared, in principle, to consider a revised and resubmitted manuscript.

    Your resubmission should include a point-by-point list of replies to all of the reviewers' comments. We strongly suggest that you carefully lay-out your point-by-point replies (each referring to page and line numbers in the revised manuscript), since they will be provided verbatim to the ensemble of the Reviewers on your submission. Please note that if you should resubmit your study, then we may choose to seek additional reports if we feel that additional expert advice is needed, or if the original reviewers are unavailable.

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    It is the policy of Ecology Letters that manuscripts be resubmitted within 3 months of the date of receipt of this letter. Please contact the Editorial Office if you are unable to submit your revision before the option expires.

    Finally, it is important to note that this letter does not pre-judge the issue of whether your paper will be finally accepted: a consensus of novelty and generality must be obtained after reassessment if your revision is to be published in our journal.

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    Yours sincerely,

    Dr Peter Thrall
    Senior Editor
    Ecology Letters


    Referees' comments to the author(s):


    Editor
    Editors Comments for the Author(s):
    The Viewpoints manuscript by Roche et al argues that “the many scientists working on evolutionary ecology of pathogens” should “shift from purely academic research towards operational research to devise practical applications…” to the covid-19 pandemic. This is the primary statement in the abstract and in the closing paragraph. Unfortunately, this position is undermined by three essential weaknesses. First, the “operational research to devise practical applications” is not defined. What should evolutionary ecologists working on pathogens start working on, and what basic research should they abandon to accomplish such a shift? Second, assuming that pathogen ecologists shifted wholesale from basic to applied research, the authors provide no guidance on what the applied research should look like and how it would prevent the next pandemic. Third, the invitation to make this shift “towards operational research more connected to the field” is not supported by any of the material presented in the remainder of the Viewpoint. The bulk of the essay describes potential environmental drivers of pathogen spillover or emergence and human behavioural factors such as encroachment into natural systems, animal husbandry, and global travel. But this is entirely unrelated to the research that scientists working on evolutionary ecology of pathogens currently do or what the authors think they should do.

    In essence, the authors advocate for a major but undefined shift in research focus for pathogen ecologists, for reasons that are not clearly described and for solutions that are not specified. I simply do not see the value of publishing such an essay and urge the authors the completely rethink what they are trying to advocate, to whom, and for what purpose.


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