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Figure 1. Bob May (Right) Chatting to Sean Nee (Left) in 1994.

Science & Society

Invasion Science andthe Global Spread ofSARS-CoV-2Martin A. Nuñez,1,*Anibal Pauchard,2,3

and Anthony Ricciardi4,5

Emerging infectious diseases, suchas coronavirus disease 2019(COVID-19), are driven by ecologicaand socioeconomic factors, andtheir rapid spread and devastatingimpacts mirror those of invasivespecies. Collaborations betweenbiomedical researchers andecologists, heretofore rare, arevital to limiting future outbreaksEnhancing the crossdisciplinaryframework offered by invasionscience could achieve this goal.

SARS-CoV-2 as a BiologicalInvasionA sinister combination of ecosystemalteration, wildlife exploitation, and globaconnectedness is increasing the risks onovel infectious disease emergence andspread [1,2]. This combination of factorsgoes far in explaining recent viraepidemics and pandemics such as severeacute respiratory syndrome coronavirus 2(SARS-CoV-2; the virus responsible foCOVID-19 disease; 2019–ongoing), Zika(2015–2016), H1N1 (2009), and SARS(2002–2004), and forewarns of others inthe future. Accordingly, societal effortsmust be directed toward managing noonly the pathogens themselves, but alsothe environmental factors that facilitatetheir emergence, spread, and impacts. Inaddition to resolving the immensesocioeconomic and cultural challengesto this goal, clearly we must develop acrossdisciplinary research program toaddress the consequences oincreasing global connectedness and

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out of a lecture to find that they hadmanaged to litter the ground floor lobbywith marigold petals. I was worried thathe would admonish me for not teachingthem better manners but instead heclapped his hands in delight.

It never occurred to Bob that he mightactually retire one day – he came into theoffice regularly and remained active in everysphere until it became impossible for himto do so. It was painful for all of us towatch such an agile mind become slowlyclouded but he was loved and looked afterby his many friends in the last years ofhis life – Paul Harvey and John Krebs, inparticular – and his constant companion ofalmost 60 years, Judith. I have left mention

of Judith till the last because she was themost special part of Bob’s life. They meton a double date while he was a postdocat Harvard and she was an undergraduateat Brandeis, married in 1962 and had adaughter, Naomi. Judith pursued a careerin publishing, and together they lived a richlife full of tender understanding towardseach other. The last time I visited Bob, hedid not seem to recognize any of us for themost part, but there was a moment whenhe took her hand and said – Judith, youare such a lovely person, I am so lucky tohave you.

1Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK

*Correspondence:sunetra.gupta@zoo.ox.ac.uk (S. Gupta).

https://doi.org/10.1016/j.tree.2020.05.010

emergentzoonotic viruses

biologicalinvasions

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Figure 1. Stages of a Zoonotic Viral Epidemic Compared with those of a Biological Invasion. Similar stage-based processes affect the spread of infectiouszoonotic pathogens (such as severe acute respiratory syndrome coronavirus 2; SARS-CoV-2) and nonpathogenic invasive organisms, demonstrating the need for acommon set of international management actions (e.g. early detection, rapid response, eradication or containment, and mitigation) appropriate to each stage of the process.

alteration of biological systems. Thiscollaborative effort must include thestudy of biological invasions, that is, thespread and proliferation of organisms innew regions.

SARS-CoV-2 should be viewed as abiological invasion, although infectioushuman diseases are rarely treated assuch. Despite the longstanding debate

on how to classify viruses as livingorganisms, this viral outbreak has traitstypical of an invasive species: suddenemergence, rapid proliferation andspread, adaptation to new environments(or hosts), large-scale geographicdispersal via human transportationnetworks, and significant impacts, in thiscase on human health and well-being. Itsmanagement requires consideration of

stage-based processes and expansionphases similar to those of invasions ononpathogenic organisms (Figure 1)Thus, we contend that the field of invasionscience [3] is positioned to contributesubstantively to understanding the driversand mechanisms of the spread, andfactors promoting outbreaks, of noveinfectious pathogens such as SARS-CoV-2.

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The Spread of Novel Organismsand the Role of Invasion ScienceInvasion science inherently examinesthe connectedness between natural andanthropogenic systems by integratingperspectives of, inter alia, ecology,biogeography, population dynamics,evolutionary biology, risk analysis,human history, and environmentalmanagement to understand the spreadand impact of introduced organisms innon-native contexts. The study ofinvasions has traditionally focused onspecies per se, but ecologists haveadvocated extending its focus moregenerally to hybrids, microbes, viruses,genetically modified organisms, andsynthetic life, which are all subject tobiological constraints, evolutionarychange, and opportunities to interfacewith global transportation networks [3–5].

A major insight from invasion scienceis that the coevolutionary relationshipsbetween introduced organisms and theirenvironments are key to understandingtheir invasion success and impact [5,6],with novel organisms (those withoutevolutionary analogues in their recipientenvironment) having the greatest potentialto cause disruption [5–7]. The introductionof novel organisms can create evolutionarymismatches in which members of therecipient community have no adaptationsto these organisms and, thus, are highlyvulnerable to their impact; the analogy todisease immunology is evident.

It is not known what proportion ofintroduced novel organisms will proliferateand cause substantial damage. Manyhave subtle or apparently minimal impactson their environment. Others can remaininnocuous for periods of time beforesuddenly becoming invasive (or virulent)in response to environmental change.Biological invasions are growing infrequency worldwide [8], and the impactsof even a small proportion (but anescalating absolute number) of these can

be so disruptive and costly that the issueis of societal importance, including tohuman health and well-being [9]. At atime of unprecedented globalization,managing the threat of invasive novelorganisms requires internationallycoordinated rapid response plans. Poorpreparedness and delayed response toinvasions can lead to inadequatebiosecurity measures and potentiallydevastating costs, as the world haswitnessed with SARS-CoV-2.

A Crossdisciplinary Approach toBiosecurityWe believe the COVID-19 pandemic canprovide a powerful impetus for ecologists,epidemiologists, sociologists, andbiomedical researchers to develop anexpanded invasion science that makesbroader contributions to global biosecurityby embracing the philosophy of the OneHealth Initiative, the goal of which is toachieve optimal public health outcomesby monitoring and managing theinteractions between humans, animals,and their environment [10]. Burgeoningstudies have combined wildlifeepidemiology with biogeography andcommunity ecology, and ecologistsrecognize the compatibility of concepts ofdisease ecology and biological invasions[11–13]. Indeed, ecological research hasrevealed complex, indirect effects thatinvasions can have on human diseaserisk [9,14]. Invasion science, a broad fielddevoted to understanding the processesbehind the spread and impact of novelorganisms, is positioned to help prevent,control, and potentially eradicate harmfulinvasive organisms, such as SARS-CoV-2, thereby allowing a more sustainablehuman existence within an increasinglyaltered natural world.

Biomedical research on emergent infectiousdiseases would benefit from what invasionscience can offer in terms of, for example, (i)a consolidated array of frameworks forstudying the consequences of eco-

evolutionary novelty, specifically the releaseof organisms lacking ecological analogues intheir recipient environments [4]; (ii) expandingknowledge of the eco-evolutionary factorsthat determine the success of transitionsbetween stages of invasion (Figure 1), whichare influenced by a combination of humanactivities, environmental conditions, and theifeedbacks [4,11,12]; and (iii) a rich literatureon the context-dependent dynamics andpredictive modeling of organismal spreadand their effects.

However, although some invasionbiologists have advocated greateintegration of their field with humanepidemiology, published evidence ocrossdisciplinary research applied toemergent infectious diseases remainsrelatively meager. Ogden and colleagues[12] noted the scarcity of examples wherethe application of human epidemiology tobiological invasions or invasion biology toemerging infectious diseases has resultedin improved prevention or controlUndoubtedly, there is a need for furtheadvancement of crossdisciplinaryapproaches toward applied research andmanagement of invasive humanpathogens.

Owing to international sharing ospatiotemporal data, the spread of SARS-CoV-2 is the most meticulously mappedbiological invasion ever documented on aglobal scale [15]. This unprecedentedrapid sharing of information, particularlyfrom the early stages of an invasion, is noonly an extraordinary opportunity foadvancing the frontiers of invasion biologyand epidemiology, but also demonstratesthe potential for global cooperation inbiosurveillance of all types of noveorganismal threat. Emerging infectiousdiseases, and invasive organisms ingeneral, are increasing in frequency withno sign of saturation [2,8] and theiprediction, prevention, and control are asocietal priority. A crossdisciplinaryinvasion science offers valuable

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underexploited frameworks and insightsthat can facilitate such initiatives and wehope that the COVID-19 pandemic willserve to catalyze greater collaboration.

AcknowledgmentsWe thank two anonymous reviewers for helpful

comments and W. Policelli for help with the figure.

A.P. was funded by CONICYT PIA AFB170008.

1Grupo de Ecología de Invasiones, INIBIOMA, CONICET,Universidad Nacional del Comahue, Pioneros 2350, San Carlosde Bariloche 8400, Argentina2Laboratorio de Invasiones Biológicas, Facultad de CienciasForestales, Universidad de Concepción, Victoria 631,Concepción, Chile3Institute of Ecology and Biodiversity (IEB), Santiago, Chile4Redpath Museum, McGill University, 859 Sherbrooke StreetWest, Montreal, QC H3A 0C4, Canada5Centre for Invasion Biology, Department of Botany andZoology, Stellenbosch University, Matieland, South Africa

*Correspondence:nunezm@gmail.com (M.A. Nuñez).

http://doi.org/10.1016/j.tree.2020.05.004

© 2020 Elsevier Ltd. All rights reserved.

References1. Afelt, A. et al. (2018) Bats, coronaviruses, and deforestation:

toward the emergence of novel infectious diseases? Front.Microbiol. 9, 702

2. Smith, K.F. et al. (2014) Global rise in humaninfectious disease outbreaks. J. R. Soc. Interface11, 20140950

3. Ricciardi, A. et al. (2017) Invasion science: a horizon scanof emerging challenges and opportunities. Trends Ecol.Evol. 32, 464–474

4. Jeschke, J.M. et al. (2013) Novel organisms: comparinginvasive species, GMOs, and emerging pathogens.Ambio 42, 541–548

5. Saul, W.C. and Jeschke, J.M. (2015) Eco-evolutionaryexperience in novel species interactions. Ecol. Lett. 18,236–245

6. Ricciardi, A. et al. (2013) Progress toward understandingthe ecological impacts of non-native species. Ecol.Monogr. 83, 263–282

7. Davis, K.T. et al. (2019) Severity of impacts of an introducedspecies correspondswith regional eco-evolutionary experience.Ecography 42, 12–22

8. Seebens, H. et al. (2017) No saturation in theaccumulation of alien species worldwide. Nat. Commun.8, 14435

9. Stoett, P. et al. (2019) Invasive alien species and planetaryand global health policy. Lancet Planet. Health 3,e400–e401

10. Destoumieux-Garzón, D. et al. (2018) The One Healthconcept: 10 years old and a long road ahead. Front. Vet.Sci. 5, 14

11. Hatcher, M.J. et al. (2012) Disease emergence andinvasions. Funct. Ecol. 26, 1275–1287

12. Ogden, N.H. et al. (2019) Emerging infectious diseasesand biological invasions: a call for a One Healthcollaboration in science and management. R. Soc. OpenSci. 6, 181577

13. Conn, D.B. (2014) Aquatic invasive species and emerginginfectious disease threats: a One Health perspective.Aquat. Invasions 9, 383–390

14. Hoyer, I.J. et al. (2017) Mammal decline, linked to invasiveBurmese python, shifts host use of vector mosquito towardsreservoir hosts of a zoonotic disease. Biol. Lett. 13, 20170353

15. Bertelsmeier, C. and Ollier, S. (2020) International trackingof the COVID-19 invasion: an amazing example of aglobalized scientific coordination effort. Biol. InvasionsPublished online May 19, 2020. http://doi.org/10.1007/s10530-020-02287-5

Book Review

Causality MeetsMathematics: In Defenseof the Mathematization ofEvolutionary BiologyJussi Lehtonen1,*

Few evolutionary biologists will besurprised by the opening statement inthis book: ‘Like any other advancedscience, contemporary evolutionarytheory is highly mathematized’ [1]. Whatmay be more surprising is the extent ofthe debate and disagreement that hassurrounded the meaning of mathematicsin evolutionary biology, spanning most ofthe past century to this day. This book –

written by a philosopher of science

closely involved with the debate – takesa perspective at the intersection ophilosophy, mathematics, and biologyWhile a practicing biologist can continuetheir research without being aware omost of the questions this book centerson, I would unreservedly recommend it toanyone with an interest in the theoreticaunderpinnings of their field.

The book can be roughly divided into twohalves. The first half provides a historicaaccount of the debate and the secondshifts the focus towards a proposedresolution. The story begins, as manystories do, with Darwin’s On the Origin oSpecies [2], notable for instigating one othe greatest scientific revolutions in historywithout the use of any explicimathematics. While mathematical work inthe early 20th century by scientists, suchas Fisher, Wright, and Haldane, solvedseveral problems Darwin’s theory had toface, new challenges of a different kindfollowed.

These challenges are exemplified by thePrice equation [3], which is – despitehaving a biological motivation – amathematical identity that is always truefor any evolving population, not reliant onempirical validation. The Price equationis thought by many to be the mosfundamental of mathematical theoremsdescribing evolutionary change [4,5]. Buif evolutionary theory is founded on amathematical identity that is an a priorlogical and mathematical truth, how can iever tell us anything new or makepredictions about the real world? Herebiology seems to profoundly differ fromphysics, which too is a mathematicascience but one in which the mathematicafoundations are not logical truths otautologies and instead rely on empiricavalidation.

The reader is introduced to the ‘receivedview’, which seems to resolve the issue

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