title: Feline Immunodeficiency Virus Cross-Species Transmission: Implications for Emergence of New Lentiviral Infections.
abstract: Owing to a complex history of host-parasite coevolution, lentiviruses exhibit a high degree of species specificity. Given the well-documented viral archeology of human immunodeficiency virus (HIV) emergence following human exposures to simian immunodeficiency virus (SIV), an understanding of processes that promote successful cross-species lentiviral transmissions is highly relevant. We previously reported natural cross-species transmission of a subtype of feline immunodeficiency virus, puma lentivirus A (PLVA), between bobcats (Lynx rufus) and mountain lions (Puma concolor) for a small number of animals in California and Florida. In this study, we investigate host-specific selection pressures, within-host viral fitness, and inter- versus intraspecies transmission patterns among a larger collection of PLV isolates from free-ranging bobcats and mountain lions. Analyses of proviral and viral RNA levels demonstrate that PLVA fitness is severely restricted in mountain lions compared to that in bobcats. We document evidence of diversifying selection in three of six PLVA genomes from mountain lions, but we did not detect selection among 20 PLVA isolates from bobcats. These findings support the hypothesis that PLVA is a bobcat-adapted virus which is less fit in mountain lions and under intense selection pressure in the novel host. Ancestral reconstruction of transmission events reveals that intraspecific PLVA transmission has occurred among panthers (Puma concolor coryi) in Florida following the initial cross-species infection from bobcats. In contrast, interspecific transmission from bobcats to mountain lions predominates in California. These findings document outcomes of cross-species lentiviral transmission events among felids that compare to the emergence of HIV from nonhuman primates.IMPORTANCECross-species transmission episodes can be singular, dead-end events or can result in viral replication and spread in the new species. The factors that determine which outcome will occur are complex, and the risk of new virus emergence is therefore difficult to predict. We used molecular techniques to evaluate the transmission, fitness, and adaptation of puma lentivirus A (PLVA) between bobcats and mountain lions in two geographic regions. Our findings illustrate that mountain lion exposure to PLVA is relatively common but does not routinely result in communicable infections in the new host. This is attributed to efficient species barriers that largely prevent lentiviral adaptation. However, the evolutionary capacity for lentiviruses to adapt to novel environments may ultimately overcome host restriction mechanisms over time and under certain ecological circumstances. This phenomenon provides a unique opportunity to examine cross-species transmission events leading to new lentiviral emergence.
authors.affiliation: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Justin
authors.initials: J
authors.lastname: Lee
authors.affiliation: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Jennifer L
authors.initials: JL
authors.lastname: Malmberg
authors.affiliation: The Pirbright Institute, Pirbright, Surrey, United Kingdom.
authors.forename: Britta A
authors.initials: BA
authors.lastname: Wood
authors.affiliation: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Sahaja
authors.initials: S
authors.lastname: Hladky
authors.affiliation: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.|Department of Biomedical Sciences, Oregon State University, Corvallis, Oregon, USA.
authors.forename: Ryan
authors.initials: R
authors.lastname: Troyer
authors.affiliation: Leidos Biomedical Research, Inc., Bethesda, Maryland, USA.
authors.forename: Melody
authors.initials: M
authors.lastname: Roelke
authors.affiliation: Florida Fish and Wildlife Conservation Commission, Gainesville, Florida, USA.
authors.forename: Mark
authors.initials: M
authors.lastname: Cunningham
authors.affiliation: Rancher's Supply Inc., Alpine, Texas, USA.
authors.forename: Roy
authors.initials: R
authors.lastname: McBride
authors.affiliation: Wildlife Health Center, University of California, Davis, Davis, California, USA.
authors.forename: Winston
authors.initials: W
authors.lastname: Vickers
authors.affiliation: Department of Pathology, Microbiology and Immunology, University of California, Davis, Davis, California, USA.
authors.forename: Walter
authors.initials: W
authors.lastname: Boyce
authors.affiliation: U.S. Geological Survey, Western Ecological Research Center, Thousand Oaks, California, USA.
authors.forename: Erin
authors.initials: E
authors.lastname: Boydston
authors.affiliation: Department of Biological Sciences, University of Cape Town, Cape Town, South Africa.|Environmental Studies Department, University of California, Santa Cruz, Santa Cruz, California, USA.
authors.forename: Laurel
authors.initials: L
authors.lastname: Serieys
authors.affiliation: Santa Monica Mountains National Recreation Area, National Park Service, Thousand Oaks, California, USA.
authors.forename: Seth
authors.initials: S
authors.lastname: Riley
authors.affiliation: Department of Fish, Wildlife, and Conservation Biology, Graduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Kevin
authors.initials: K
authors.lastname: Crooks
authors.affiliation: Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA sue.vandewoude@colostate.edu.
authors.forename: Sue
authors.initials: S
authors.lastname: VandeWoude
mesh_terms: D000818:Animals; D002140:California / Q000453:epidemiology; D002371:Cat Diseases / Q000453:epidemiology / Q000635:transmission / Q000821:virology*; D002415:Cats; D005260:Female; D005431:Florida / Q000453:epidemiology; D016089:Immunodeficiency Virus, Feline / Q000502:physiology*; D046008:Lynx / Q000821:virology*; D008297:Male; D010802:Phylogeny; D011110:Polymorphism, Genetic; D046011:Puma / Q000821:virology*; D012641:Selection, Genetic; D013045:Species Specificity; D056189:Viral Tropism
keywords: bobcat; cross-species transmission; feline; feline immunodeficiency virus; mountain lion; retroviruses