Phylogeographical and cross‐species transmission dynamics of SAT1 and SAT2 foot‐and‐mouth disease virus in Eastern Africa

Understanding the dynamics of foot‐and‐mouth disease virus (FMDV), an endemic and economically constraining disease, is critical in designing control programmes in Africa. This study investigates the evolutionary epidemiology of SAT1 and SAT2 FMDV in Eastern Africa, as well as between cattle and wild African buffalo. Bayesian phylodynamic models were used to analyse SAT1 and SAT2 VP1 gene segments collected between 1975 and 2016, focusing on the SAT1 and SAT2 viruses currently circulating in Eastern Africa. The root state posterior probabilities inferred from our analyses suggest Zimbabwe as the ancestral location for SAT1 currently circulating in Eastern Africa (p = 0.67). For the SAT2 clade, Kenya is inferred to be the ancestral location for introduction of the virus into other countries in Eastern Africa (p = 0.72). Salient (Bayes factor >10) viral dispersal routes were inferred from Tanzania to Kenya, and from Kenya to Uganda for SAT1 and SAT2, respectively. Results suggest that cattle are the source of the SAT1 and SAT2 clades currently circulating in Eastern Africa. In addition, our results suggest that the majority of SAT1 and SAT2 in livestock come from other livestock rather than wildlife, with limited evidence that buffalo serve as reservoirs for cattle. Insights from the present study highlight the role of cattle movements and anthropogenic activities in shaping the evolutionary history of SAT1 and SAT2 in Eastern Africa. While the results may be affected by inherent limitations of imperfect surveillance, our analysis elucidates the dynamics between host species in this region, which is key to guiding disease intervention activities.

[1]  Andrés Perez,et al.  The role of African buffalo in the epidemiology of foot-and-mouth disease in sympatric cattle and buffalo populations in Kenya , 2018 .

[2]  S. Cleaveland,et al.  Waves of endemic foot-and-mouth disease in eastern Africa suggest feasibility of proactive vaccination approaches , 2018, Nature Ecology & Evolution.

[3]  S. Lycett,et al.  Phylogeographic analysis and identification of factors impacting the diffusion of Foot-and-Mouth disease virus in Africa , 2018, bioRxiv.

[4]  G. Belsham,et al.  Molecular epidemiology, evolution and phylogeny of foot-and-mouth disease virus. , 2018, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[5]  C. Wright,et al.  Full Genome Sequencing Reveals New Southern African Territories Genotypes Bringing Us Closer to Understanding True Variability of Foot-and-Mouth Disease Virus in Africa , 2018, Viruses.

[6]  D. Paton,et al.  Genetic and antigenic characterization of serotype O FMD viruses from East Africa for the selection of suitable vaccine strain , 2017, Vaccine.

[7]  M. Suchard,et al.  Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak , 2017, bioRxiv.

[8]  Matthew Scotch,et al.  Bayesian phylogeography of influenza A/H3N2 for the 2014-15 season in the United States using three frameworks of ancestral state reconstruction , 2017, PLoS Comput. Biol..

[9]  Neil J. Anderson,et al.  Genomics reveals historic and contemporary transmission dynamics of a bacterial disease among wildlife and livestock , 2016, Nature Communications.

[10]  M. Suchard,et al.  SpreaD3: Interactive Visualization of Spatiotemporal History and Trait Evolutionary Processes. , 2016, Molecular biology and evolution.

[11]  Andrés Perez,et al.  Transmission of Foot-and-Mouth Disease SAT2 Viruses at the Wildlife–Livestock Interface of Two Major Transfrontier Conservation Areas in Southern Africa , 2016, Front. Microbiol..

[12]  R. Moormann,et al.  Foot-and-mouth Disease Transmission in Africa: Implications for Control, a Review. , 2016, Transboundary and emerging diseases.

[13]  Hyeyoung Kim,et al.  Simulating the Transmission of Foot-And-Mouth Disease Among Mobile Herds in the Far North Region, Cameroon , 2016, J. Artif. Soc. Soc. Simul..

[14]  S. Gubbins,et al.  Differential Persistence of Foot-and-Mouth Disease Virus in African Buffalo Is Related to Virus Virulence , 2016, Journal of Virology.

[15]  R. Morrison,et al.  Applications of Bayesian Phylodynamic Methods in a Recent U.S. Porcine Reproductive and Respiratory Syndrome Virus Outbreak , 2016, Front. Microbiol..

[16]  H. Siegismund,et al.  Unrecognized circulation of SAT 1 foot-and-mouth disease virus in cattle herds around Queen Elizabeth National Park in Uganda , 2016, BMC Veterinary Research.

[17]  Andrew Rambaut,et al.  Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen) , 2016, Virus evolution.

[18]  Rasmus Heller,et al.  Time Clustered Sampling Can Inflate the Inferred Substitution Rate in Foot-And-Mouth Disease Virus Analyses , 2015, PloS one.

[19]  Hyeyoung Kim,et al.  Serotype-Specific Transmission and Waning Immunity of Endemic Foot-and-Mouth Disease Virus in Cameroon , 2015, PloS one.

[20]  Nicola De Maio,et al.  New Routes to Phylogeography: A Bayesian Structured Coalescent Approximation , 2015, PLoS genetics.

[21]  D. Beltrán-Alcrudo,et al.  Global trends in infectious diseases at the wildlife–livestock interface , 2015, Proceedings of the National Academy of Sciences.

[22]  D. Berkvens,et al.  Risk factors for foot-and-mouth disease in Tanzania, 2001-2006. , 2015, Transboundary and emerging diseases.

[23]  H. Siegismund,et al.  Foot-and-Mouth Disease Virus Serotype SAT 3 in Long-Horned Ankole Calf, Uganda , 2015, Emerging infectious diseases.

[24]  Anders Larsson,et al.  AliView: a fast and lightweight alignment viewer and editor for large datasets , 2014, Bioinform..

[25]  Ellen Brooks-Pollock,et al.  A dynamic model of bovine tuberculosis spread and control in Great Britain , 2014, Nature.

[26]  C. Donnelly,et al.  Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis , 2014, Proceedings of the National Academy of Sciences.

[27]  M. Suchard,et al.  Unifying Viral Genetics and Human Transportation Data to Predict the Global Transmission Dynamics of Human Influenza H3N2 , 2014, PLoS pathogens.

[28]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[29]  Matthew Scotch,et al.  Phylogeography of influenza A H5N1 clade 2.2.1.1 in Egypt , 2013, BMC Genomics.

[30]  A. Rambaut,et al.  Reconstructing Geographical Movements and Host Species Transitions of Foot-and-Mouth Disease Virus Serotype SAT 2 , 2013, mBio.

[31]  J. Hopcraft,et al.  Evaluating the Potential for the Environmentally Sustainable Control of Foot and Mouth Disease in Sub-Saharan Africa , 2013, EcoHealth.

[32]  T. Boulinier,et al.  Contacts and foot and mouth disease transmission from wild to domestic bovines in Africa , 2013 .

[33]  Mandev S. Gill,et al.  Improving Bayesian population dynamics inference: a coalescent-based model for multiple loci. , 2013, Molecular biology and evolution.

[34]  Michel de Garine-Wichatitsky,et al.  Relationship between burden of infection in ungulate populations and wildlife/livestock interfaces , 2013, Epidemiology and Infection.

[35]  M. Suchard,et al.  Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. , 2012, Molecular biology and evolution.

[36]  A. Michel,et al.  The African buffalo: a villain for inter-species spread of infectious diseases in southern Africa. , 2012, The Onderstepoort journal of veterinary research.

[37]  R. Lanfear,et al.  Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. , 2012, Molecular biology and evolution.

[38]  M. Suchard,et al.  Bayesian Phylogenetics with BEAUti and the BEAST 1.7 , 2012, Molecular biology and evolution.

[39]  Eric F. Lambin,et al.  The landscape epidemiology of foot-and-mouth disease in South Africa: A spatially explicit multi-agent simulation , 2011 .

[40]  J. Treanor,et al.  Management of Yellowstone bison and brucellosis transmission risk – Implications for conservation and restoration , 2011 .

[41]  Heebal Kim,et al.  Phylogenomics and molecular evolution of foot-and-mouth disease virus , 2011, Molecules and cells.

[42]  H. Siegismund,et al.  The role of African buffalos (syncerus caffer) in the maintenance of foot-and-mouth disease in Uganda , 2010, BMC veterinary research.

[43]  H. Siegismund,et al.  Evolutionary analysis of foot-and-mouth disease virus serotype SAT 1 isolates from east africa suggests two independent introductions from southern africa , 2010, BMC Evolutionary Biology.

[44]  Ming-Hui Chen,et al.  Choosing among Partition Models in Bayesian Phylogenetics , 2010, Molecular biology and evolution.

[45]  Vincent Moulton,et al.  RDP3: a flexible and fast computer program for analyzing recombination , 2010, Bioinform..

[46]  H. Siegismund,et al.  Patterns, risk factors and characteristics of reported and perceived foot-and-mouth disease (FMD) in Uganda , 2010, Tropical Animal Health and Production.

[47]  B. Charleston,et al.  Options for control of foot-and-mouth disease: knowledge, capability and policy , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Alexei J. Drummond,et al.  Bayesian Phylogeography Finds Its Roots , 2009, PLoS Comput. Biol..

[49]  I. Olsen,et al.  Neutralization of Interleukin-10 from CD14+ Monocytes Enhances Gamma Interferon Production in Peripheral Blood Mononuclear Cells from Mycobacterium avium subsp. paratuberculosis-Infected Goats , 2009, Clinical and Vaccine Immunology.

[50]  M. Suchard,et al.  Learning to count: robust estimates for labeled distances between molecular sequences. , 2009, Molecular biology and evolution.

[51]  P. Daszak,et al.  Wildlife–livestock conflict: the risk of pathogen transmission from bison to cattle outside Yellowstone National Park , 2009 .

[52]  Marco A. R. Ferreira,et al.  Bayesian analysis of elapsed times in continuous‐time Markov chains , 2008 .

[53]  M. Suchard,et al.  Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. , 2008, Molecular biology and evolution.

[54]  O. Pybus,et al.  Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. , 2008, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[55]  R. Kock,et al.  Serological Survey for Foot-and-Mouth Disease Virus in Wildlife in Eastern Africa and Estimation of Test Parameters of a Nonstructural Protein Enzyme-Linked Immunosorbent Assay for Buffalo , 2008, Clinical and Vaccine Immunology.

[56]  J. Valarcher,et al.  Epidemiological patterns of foot-and-mouth disease worldwide. , 2008, Transboundary and emerging diseases.

[57]  K. Rich,et al.  Poverty impacts of foot-and-mouth disease and the poverty reduction implications of its control , 2007, Veterinary Record.

[58]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[59]  E. C. Anderson,et al.  An investigation into the source and spread of foot and mouth disease virus from a wildlife conservancy in Zimbabwe. , 2004, Revue scientifique et technique.

[60]  高山 康夫.  Strain , 2004, Definitions.

[61]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[62]  P. Sutmoller.  The Fencing Issue Relative to the Control of Foot‐and‐Mouth Disease , 2002, Annals of the New York Academy of Sciences.

[63]  E. Domingo,et al.  Foot-and-mouth disease virus. , 2002, Comparative immunology, microbiology and infectious diseases.

[64]  Alexei J Drummond,et al.  Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. , 2002, Genetics.

[65]  L. H. Taylor,et al.  Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[66]  G. Thomson,et al.  Natural transmission of foot-and-mouth disease virus between African buffalo (Syncerus caffer) and impala (Aepyceros melampus) in the Kruger National Park, South Africa , 2000, Epidemiology and Infection.

[67]  R. Kitching.  A recent history of foot-and-mouth disease. , 1998, Journal of comparative pathology.

[68]  S. Tavaré,et al.  Ancestral Inference in Population Genetics , 1994 .

[69]  J. L. Montagne,et al.  Emerging infectious diseases. , 1994, The Journal of infectious diseases.

[70]  K. Sorensen,et al.  Experimental transmission of foot-and-mouth disease virus from carrier African buffalo (Syncerus caffer) to cattle in Zimbabwe , 1994, Veterinary Record.

[71]  S. Golding,et al.  Infection of some species of African wild life with foot-and-mouth disease virus. , 1972, Journal of comparative pathology.

[72]  R. A. Leibler,et al.  On Information and Sufficiency , 1951 .

[73]  B. McCowan,et al.  Quantifying microbe transmission networks for wild and domestic ungulates in Kenya , 2014 .

[74]  H. Siegismund,et al.  Genetic diversity of serotype A foot-and-mouth disease viruses in Kenya from 1964 to 2013; implications for control strategies in eastern Africa. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[75]  N. Faria,et al.  Phylogeography of foot-and-mouth disease virus serotype O in Ecuador. , 2013, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[76]  W. Vosloo,et al.  A qualitative risk assessment of factors contributing to foot and mouth disease cattle outbreaks along the western boundary of the Kruger National Park , 2009 .

[77]  Y. Aklilu.  Livestock Marketing in Kenya and Ethiopia: A Review of Policies and Practice , 2008 .

[78]  C. Hamblin,et al.  The duration of the foot-and-mouth disease virus carrier state in African buffalo (i) in the individual animal and (ii) in a free-living herd. , 1985, Comparative immunology, microbiology and infectious diseases.

[79]  J. Kingman.  On the genealogy of large populations , 1982, Journal of Applied Probability.

[80]  W. B.,et al.  Foot and mouth disease. , 2002, Research in veterinary science.