Bridging Taxonomic and Disciplinary Divides in Inf

Authors: Elizabeth T Borer Janis Antonovics Linda L Kinkel Peter J Hudson Peter Daszak Matthew J Ferrari Karen A Garrett Colin R Parrish Andrew F Read David M Rizzo

Publish Date: 2011/11/16

Volume: 8, Issue: 3, Pages: 261-267

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Abstract

Pathogens traverse disciplinary and taxonomic boundaries yet infectious disease research occurs in many separate disciplines including plant pathology veterinary and human medicine and ecological and evolutionary sciences These disciplines have different traditions goals and terminology creating gaps in communication Bridging these disciplinary and taxonomic gaps promises novel insights and important synergistic advances in control of infectious disease An approach integrated across the plantanimal divide would advance our understanding of disease by quantifying critical processes including transmission community interactions pathogen evolution and complexity at multiple spatial and temporal scales These advances require more substantial investment in basic disease researchPathogens do not respect disciplinary or taxonomic boundaries However infectious disease research has been and still is the province of many separate disciplines including veterinary medicine plant pathology and human medicine where these fields are defined by the host organism being studied rather than by the concepts that cut across taxonomic boundaries In the past decade infectious disease research also has captured the full attention of the ecological and evolutionary sciences These disciplines each have different traditions different goals and often quite different terminology creating significant gaps in communication For example the word ‘virulence’ is defined differently by plant pathologists evolutionary biologists and medical doctors similarly the term ‘drift’ evokes quite different processes for a population geneticist and a researcher of influenza Terminological inconsistency is only a symptom of larger divides and it is clear that bridging these disciplinary and taxonomic gaps to allow true interdisciplinary research efforts will lead to novel insights important synergistic interactions across fields and advanced understanding and ability to control infectious diseaseA truly interdisciplinary approach will hasten understanding leading to novel insights that will benefit all of the disciplines involved In particular an approach which is agnostic to the taxonomy of the host focusing on the fundamental ecological and evolutionary processes inherent to a pathogenic lifestyle eg transmission host immune or other defenses virulence or species interactions promises rapid conceptual and technical advances Further by employing a comparative approach that is inclusive of microorganisms plants wild and domestic animals and humans we will deepen our understanding of disease for all of these fields The exchange of specific techniques and quantitative tools also will open up approaches for dealing with complexity at multiple spatial and temporal scales Infectious disease in humans and in plant and animal agriculture or in domesticated companion animals is often the direct consequence of interactions with nonagricultural populations of the same hosts Cleaveland et al 2001 Taylor et al 2001 Anderson et al 2004 Parrish et al 2008 Achieving an understanding of transmission and evolutionary dynamics in both wild and domesticated hosts will offer novel solutions to emerging infectious disease challenges For example this type of approach has proven successful in advancing our understanding of two recent emerging diseases white nose syndrome in bats and chytridiomycosis in frogs Berger et al 1998 Blehert et al 2009 In both cases longterm expertise in the pathology and ecology of fungal pathogens of plants allowed the efficient identification of these extremely significant fungal pathogens of wildlife The study of plant sexually transmitted diseases also has stimulated increased understanding of sexually transmitted diseases in animals and humans Lockhart et al 1996 including the role played by basal immune system functioning Nunn et al 2000Fundamental epidemiological problems can be addressed and illuminated by gathering data across many systems For example a general understanding of the accelerating nature of epidemic spread has arisen from a multispecies approach Mundt et al 2009 Similarly wellunderstood principles in one area can provide critical insights in another For example genetic variation in host resistance is commonly considered in plant pathology but is less often explicitly considered in studies of animal diseases While it is hard to judge issues from hindsight we posit that if the medical research community when confronted with the early stages of the AIDS epidemic had been as aware of genetic variation in host resistance to pathogens as the average plant pathologist the understanding of the pathology of HIV and the development of antiviral therapies based on this knowledge would have advanced far more rapidly Pettipher and Cardon 2002 Lederman et al 2006 Communication across this divide could have changed historyThe science of infectious disease is poised for enormous advances if scientists can communicate collaborate and synthesize across organismal and conceptual divides Here we provide examples of concepts and techniques spanning disciplinary divides where combining the common approaches taken to understand plant animal and human disease could generate strong synergy and we argue that such translational science requires active investment in truly interdisciplinary programs by funding agenciesThe principles underlying pathogen dispersal among hosts and epidemics are shared across animal and plant hosts Mundt et al 2009 and control strategies for both plant and animal pathogens can be mutually informative For example Asiatic citrus canker an infection caused by the bacterium Xanthomonas citri subsp citri produces bacteriumleaking lesions on leaves and fruit which are harmless to humans but are unsightly and dramatically reduce the economic value of infected citrus Gottwald et al 2002a By providing information on critical parameters to stem an epidemic the mathematical models of the spread of foot and mouth disease FMDV that have been developed to inform the control of outbreaks in European livestock eg Keeling et al 2003 Haydon et al 2004 could have provided information to guide control strategies for plant pathogen outbreaks like citrus canker in Florida Schubert et al 2001 Gottwald et al 2002b Further the lessons learned from the coordinated response between individual producers industry and national agencies to implement policy and response to FMDV outbreaks Haydon et al 2004 are key components for evaluation of practical control strategies for citrus canker and other largescale agricultural pathogens For example FMDV data now exist on the social biological and economic effects of ring culling culling of apparently uninfected herds and bans on livestock movement all of which could be used for developing more effective strategies to control the transmission of other plant and animal diseasesIn addition predicting the scaling of epidemic processes from local to continental levels remains a challenge because of a paucity of examples within any individual host taxa ie humans livestock wildlife crops The handful of welldocumented continental scale outbreaks eg influenza in humans Viboud et al 2006 rabies in raccoons Smith et al 2002 soybean rust Isard et al 2005 and sudden oak death Meentemeyer et al 2008 have revealed that locally homogeneous transmission dynamics give way to strongly heterogeneous transmission patterns at the continental scale that are dominated by a combination of local environmental suitability Isard et al 2005 Meentemeyer et al 2008 host movement patterns Smith et al 2002 Viboud et al 2006 or atmospheric currents Isard et al 2005 Novel methods combining transmission models geographic information system GIS and remote sensing to quantify risk of outbreaks and predict disease spread in plant pathogens Meentemeyer et al 2004 Mumma et al 2009 can be adapted to address other threats at the national level and experimental work on pathogens such as sudden oak death or wheat rusts Mundt et al 2009 Meentemeyer et al 2011 promises significant advances in predicting regional or nationalscale infectious disease spread Given the limited number of continental or global scale epidemics that can be studied understanding the role of local and regional controls on transmission dynamics would clearly benefit from a comparative approach that is agnostic to host taxonomy Containing any emerging infectious disease newly introduced or evolved pathogen bioterror or agroterror agent will benefit from recognition of the similarities among pathogens infecting animal and plant hosts and rapid efficient communication among researchers in different disciplines to effectively translate such models into recommendations that can aid decision makersA major challenge in the study of infectious diseases is to explain the large variation in the response of hosts to infection from those that exhibit no disease symptoms to those that die rapidly or result in exceptionally high levels of transmission super spreaders These variable responses have important repercussions for identifying and predicting disease spread and consequently for developing and implementing intervention methods Though behavioral physiological and genetic determinants of variation in susceptibility have been wellstudied recent work in both medicine and agriculture suggests that variation in host health and resistance to novel microbes may also be caused by community level ecological interactions among different microbes The vast majority of microbes are not pathogenic and thus pathogen infection in many cases is akin to the invasion of a novel microbe into an existing community within a host Current work in both plant and animal hosts is revealing that colonies of microbes can produce antimicrobial compounds that protect against infection or colonization by unrelated pathogens Conn et al 2008 Harris et al 2009 Verma et al 2009 Bacteriotherapy is a new and extremely promising manipulation of microbes in humans to control disease Khoruts et al 2010 Through closer communication these parallel inquiries and novel findings in both plants and animals have great potential to develop powerful new “biocontrol” tools for both humans and agriculture especially given the ubiquitous problem of rapid evolution of resistance to antimicrobial agents

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