A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus

Emerging pathogens potentially undergo rapid evolution while expanding in population size and geographic range during the course of invasion, yet it is generally difficult to demonstrate how these processes interact. Our analysis of a 30-yr data set covering a large-scale rabies virus outbreak among North American raccoons reveals the long lasting effect of the initial infection wave in determining how viral populations are genetically structured in space. We further find that coalescent-based estimates derived from the genetic data yielded an amazingly accurate reconstruction of the known spatial and demographic dynamics of the virus over time. Our study demonstrates the combined evolutionary and population dynamic processes characterizing the spread of pathogen after its introduction into a fully susceptible host population. Furthermore, the results provide important insights regarding the spatial scale of rabies persistence and validate the use of coalescent approaches for uncovering even relatively complex population histories. Such approaches will be of increasing relevance for understanding the epidemiology of emerging zoonotic diseases in a landscape context.

[1]  D. Slate,et al.  Status of oral rabies vaccination in wild carnivores in the United States. , 2005, Virus research.

[2]  P. Daszak,et al.  Emerging infectious diseases of wildlife--threats to biodiversity and human health. , 2000, Science.

[3]  Grenfell,et al.  Persistence thresholds for phocine distemper virus infection in harbour seal Phoca vitulina metapopulations , 1998 .

[4]  David L Smith,et al.  A priori prediction of disease invasion dynamics in a novel environment , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  Eli Stahl,et al.  Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  David L Smith,et al.  Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Shigesada,et al.  Biological Invasions: Theory and Practice , 1997 .

[8]  Seraina Klopfstein,et al.  The fate of mutations surfing on the wave of a range expansion. , 2006, Molecular biology and evolution.

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

[10]  T. F. Hansen,et al.  Phylogenies and the Comparative Method: A General Approach to Incorporating Phylogenetic Information into the Analysis of Interspecific Data , 1997, The American Naturalist.

[11]  C. Bult,et al.  TESTING SIGNIFICANCE OF INCONGRUENCE , 1994 .

[12]  Christopher A. Edmonds,et al.  Mutations arising in the wave front of an expanding population. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  D. Stallknecht,et al.  Mycoplasmal conjunctivitis in wild songbirds: the spread of a new contagious disease in a mobile host population. , 1997, Emerging infectious diseases.

[14]  C. Bult,et al.  ForumTesting Significance of Incongruence , 1994 .

[15]  J. Childs,et al.  Environmental and Human Demographic Features Associated with Epizootic Raccoon Rabies in Maryland, Pennsylvania, and Virginia , 2003, Journal of wildlife diseases.

[16]  C. Rupprecht,et al.  Raccoon rabies: the re-emergence of an epizootic in a densely populated area , 1994 .

[17]  Ziheng Yang,et al.  PAML: a program package for phylogenetic analysis by maximum likelihood , 1997, Comput. Appl. Biosci..

[18]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[19]  L. Real,et al.  Spatial dynamics and molecular ecology of North American rabies. , 2005, The Journal of heredity.

[20]  S. Riley,et al.  Population density, survival, and rabies in raccoons in an urban national park , 1998 .

[21]  W. Huang,et al.  The design of strain-specific polymerase chain reactions for discrimination of the racoon rabies virus strain from indigenous rabies viruses of Ontario. , 1996, Journal of Virological Methods.

[22]  Alexei J Drummond,et al.  Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. , 2006, Molecular biology and evolution.

[23]  E. Holmes,et al.  Genetic constraints and the adaptive evolution of rabies virus in nature. , 2002, Virology.

[24]  A. Drummond,et al.  A Virus Reveals Population Structure and Recent Demographic History of Its Carnivore Host , 2006, Science.

[25]  Andrew Rambaut,et al.  Estimating the rate of molecular evolution: incorporating non-contemporaneous sequences into maximum likelihood phylogenies , 2000, Bioinform..

[26]  A. Rodrigo,et al.  Measurably evolving populations , 2003 .

[27]  J. Avise Phylogeography: The History and Formation of Species , 2000 .

[28]  O. Pybus,et al.  The Epidemic Behavior of the Hepatitis C Virus , 2001, Science.

[29]  Edward C Holmes,et al.  The phylogeography of human viruses , 2004, Molecular ecology.

[30]  L. Matthews,et al.  Low-coverage vaccination strategies for the conservation of endangered species , 2006, Nature.

[31]  O. Pybus,et al.  Bayesian coalescent inference of past population dynamics from molecular sequences. , 2005, Molecular biology and evolution.

[32]  David L. Smith,et al.  Assessing the role of long-distance translocation and spatial heterogeneity in the raccoon rabies epidemic in Connecticut , 2005, Preventive Veterinary Medicine.

[33]  L. Real,et al.  Spatiotemporal analysis of epizootic raccoon rabies propagation in Connecticut, 1991-1995. , 2002, Vector borne and zoonotic diseases.

[34]  O N Bjørnstad,et al.  Predicting the local dynamics of epizootic rabies among raccoons in the United States. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  C. Dye,et al.  Immunization coverage required to prevent outbreaks of dog rabies. , 1996, Vaccine.

[36]  J. Childs,et al.  Rabies epizootics among raccoons vary along a North-South gradient in the Eastern United States. , 2001, Vector borne and zoonotic diseases.

[37]  B T Grenfell,et al.  Individual-based perspectives on R(0). , 2000, Journal of theoretical biology.