University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln U.S. Department of Agriculture: Agricultural Publications from USDA-ARS / UNL Faculty Research Service, Lincoln, Nebraska 2-2013 Frequent Cross-Species Transmission of Parvoviruses among Diverse Carnivore Hosts Andrew B. Allison Cornell University Dennis J. Kohler USDA-APHIS-WS, [email protected] Karen A. Fox Colorado Division of Parks and Wildlife Justin D. Brown University of Georgia, [email protected] Richard W. Gerhold University of Tennessee Institute of Agriculture, [email protected] See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/usdaarsfacpub Allison, Andrew B.; Kohler, Dennis J.; Fox, Karen A.; Brown, Justin D.; Gerhold, Richard W.; Shearn-Bochsler, Valerie I.; Dubovi, Edward J.; Parrish, Colin R.; and Holmes, Edward C., "Frequent Cross-Species Transmission of Parvoviruses among Diverse Carnivore Hosts" (2013). Publications from USDA-ARS / UNL Faculty. 1260. https://digitalcommons.unl.edu/usdaarsfacpub/1260 This Article is brought to you for free and open access by the U.S. Department of Agriculture: Agricultural Research Service, Lincoln, Nebraska at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Publications from USDA-ARS / UNL Faculty by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Andrew B. Allison, Dennis J. Kohler, Karen A. Fox, Justin D. Brown, Richard W. Gerhold, Valerie I. Shearn- Bochsler, Edward J. Dubovi, Colin R. Parrish, and Edward C. Holmes This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/ usdaarsfacpub/1260 Frequent Cross-Species Transmission of Parvoviruses among Diverse Carnivore Hosts Andrew B. Allison,a Dennis J. Kohler,b Karen A. Fox,c Justin D. Brown,d Richard W. Gerhold,e Valerie I. Shearn-Bochsler,f Edward J. Dubovi,g Colin R. Parrish,a Edward C. Holmesh,i* Baker Institute for Animal Health, Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, New York, USAa; USDA-APHIS- WS/National Wildlife Research Center, Fort Collins, Colorado, USAb; Colorado Division of Parks and Wildlife, Wildlife Health Program, Fort Collins, Colorado, USAc; Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, University of Georgia, Athens, Georgia, USAd; Center for Wildlife Health, Department of Forestry, Wildlife and Fisheries, University of Tennessee Institute of Agriculture, Knoxville, Tennessee, USAe; United States Geological Survey, National Wildlife Health Center, Madison, Wisconsin, USAf; Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, New York, USAg; Center for Infectious Disease Dynamics, Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, USAh; Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USAi Although parvoviruses are commonly described in domestic carnivores, little is known about their biodiversity in nondomestic species. A phylogenetic analysis of VP2 gene sequences from puma, coyote, gray wolf, bobcat, raccoon, and striped skunk re- vealed two major groups related to either feline panleukopenia virus (“FPV-like”) or canine parvovirus (“CPV-like”). Cross- species transmission was commonplace, with multiple introductions into each host species but, with the exception of raccoons, relatively little evidence for onward transmission in nondomestic species. etermining how viruses infect and spread in new host species resulting in loss of the canine host range and altering neutralizing Dis central to the study of disease emergence (1, 2). The spread antibody epitopes (17, 18). of canine parvovirus (CPV) in dogs during the late 1970s is one of To further clarify virus-host relationships, we characterized the best documented examples of viral emergence leading to a parvoviruses that circulate in several species of wild carnivore in pandemic in a new host (3). It has been widely assumed that the the United States, determining those which represent viable hosts new canine virus (initially known as CPV-2) emerged in dogs for parvoviruses by sustaining prolonged viral transmission and following the cross-species transfer of feline panleukopenia virus those in which parvovirus infections are apparently transient spill- (FPV) from cats or a related carnivore host (2, 4, 5). Comparing overs. Accordingly, we sampled 58 novel parvoviruses from either isolates of FPV and CPV has provided important insights into the free-ranging (gray wolf, coyote, bobcat, puma, striped skunk, and viral mutations controlling host range and how different interac- raccoon) or wild species that were brought into captive outdoor tions with the host transferrin receptor type-1 (TfR) enabled both facilities for rehabilitation (raccoon) or containment (gray adaptation to dogs and the later evolution of the CPV-2a, CPV-2b, [Mexican] wolf) purposes (Table 1). All new FPV and CPV se- and CPV-2c variants that exhibit characteristic differences in an- quences were obtained from carnivores that either were showing tigenic sites and in cell tropism (3, 6, 7). typical clinical signs of parvovirus infection (e.g., hemorrhagic A variety of host species other than domestic cats and dogs enteritis) or were asymptomatic, suggestive of either an active but harbor closely related parvoviruses, and it has become increas- subclinical infection or recovery from a previous infection in ingly apparent that nondomestic animals are commonly infected, which persistent DNA could be detected in tissues. The detection even though little disease is observed in many cases (8–12). How- of viral DNA in animals without active infection is likely due to ever, those parvoviruses previously detected in a variety of other residual DNA in tissues after virus was inactivated by the host species, including many different large cats, raccoons, raccoon immune response and parallels the results reported for lifelong dogs, arctic foxes, and mink, often represent opportunistic sam- residual DNA of human parvoviruses (19), as well as recent re- ples obtained from animals in artificial settings such as zoos or fur ports of persistent DNA in cats (20). In most cases, tissue samples (gastrointestinal tract, mesenteric lymph node, spleen, tongue, or farms (13–15), with the majority of these viruses falling into a 3 single FPV-like clade distinct from CPV in dogs (4, 16). More feces) approximately 0.5 mm in size were placed in 1.5-ml micro- centrifuge tubes and stored at Ϫ20°C until further processing. recently, raccoons from a variety of locations in the United States DNA was extracted from tissues using a commercial kit (Qiagen, have been shown to commonly harbor parvoviruses, which they have likely been associated with for at least 20 years (17). Notably, most raccoon parvovirus sequences, as well as a single isolate from Received 5 September 2012 Accepted 28 November 2012 a bobcat, fell in intermediate locations between the dog-associated Published ahead of print 5 December 2012 CPV-2 and CPV-2a strains in a phylogenetic tree of the VP2 pro- Address correspondence to Edward C. Holmes, [email protected]. tein (17). Hence, raccoon parvoviruses may have played a central * Present address: Sydney Emerging Infections and Biosecurity Institute, School of role in the transition between CPV-2 and the later CPV-2a, -2b, Biological Sciences and Sydney Medical School, The University of Sydney, Sydney, and -2c variants that not only infected dogs but regained the abil- NSW, Australia. ity to infect cats (a property lost in CPV-2). Indeed, the CPV-like Copyright © 2013, American Society for Microbiology. All Rights Reserved. viruses from raccoons possess multiple amino acid changes on the doi:10.1128/JVI.02428-12 surface of their capsids that affect binding to the host-specific TfR, 2342 jvi.asm.org Journal of Virology p. 2342–2347 February 2013 Volume 87 Number 4 Phylogenetic Diversity of Carnivore Parvoviruses TABLE 1 Carnivore parvoviruses sequenced and analyzed in this study GenBank Isolate Virus Host County State Yr accession no. CPV-2b/Gray wolf/AZ/16382-01/99 CPV-like Canis lupus baileyi Greenlee Arizona 1999 JX475240 CPV-2b/Gray wolf/NM/16401-01/99 CPV-like Canis lupus baileyi Socorro New Mexico 1999 JX475241 CPV-2b/Gray wolf/WI/18268/02 CPV-like Canis lupus nubilus Langlade Wisconsin 2002 JX475242 CPV-2c/Gray wolf/ID/22772/09 CPV-like Canis lupus occidentalis Camas Idaho 2009 JX475243 CPV-2b/Puma/CO/2235/09 CPV-like Puma concolor Douglas Colorado 2009 JX475251 FPV/Puma/CO/952/10 FPV-like Puma concolor Yuma Colorado 2010 JX475245 CPV/Puma/CO/2503/10 CPV-like Puma concolor Larimer Colorado 2010 JX475246 CPV-2b/Puma/CO/1246/10 CPV-like Puma concolor Jefferson Colorado 2010 JX475247 CPV-2b/Puma/CO/898/10 CPV-like Puma concolor Larimer Colorado 2010 JX475249 CPV-2b/Puma/CO/728/10 CPV-like Puma concolor Larimer Colorado 2010 JX475250 CPV-2c/Puma/CO/1316/10 CPV-like Puma concolor Boulder Colorado 2010 JX475252 FPV/Puma/CO/546/10 FPV-like Puma concolor Jefferson Colorado 2010 JX475253 FPV/Puma/CO/977/10 FPV-like Puma concolor Clear Creek Colorado 2010 JX475254 CPV-2b/Puma/CO/1237/10 CPV-like Puma concolor Weld Colorado 2010 JX475257 CPV/Puma/CO/1321/10 CPV-like Puma concolor Larimer Colorado 2010 JX475258 FPV/Puma/CO/545/10 FPV-like Puma concolor Chaffee Colorado 2010 JX475259 CPV-2c/Puma/CO/704/10