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J Virol. 2017 Feb 14;91(5). pii: e02134-16. doi: 10.1128/JVI.02134-16. Print 2017 Mar 1.

Feline Immunodeficiency Virus Cross-Species Transmission: Implications for Emergence of New Lentiviral Infections.

Author information

1
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
2
The Pirbright Institute, Pirbright, Surrey, United Kingdom.
3
Department of Biomedical Sciences, Oregon State University, Corvallis, Oregon, USA.
4
Leidos Biomedical Research, Inc., Bethesda, Maryland, USA.
5
Florida Fish and Wildlife Conservation Commission, Gainesville, Florida, USA.
6
Rancher's Supply Inc., Alpine, Texas, USA.
7
Wildlife Health Center, University of California, Davis, Davis, California, USA.
8
Department of Pathology, Microbiology and Immunology, University of California, Davis, Davis, California, USA.
9
U.S. Geological Survey, Western Ecological Research Center, Thousand Oaks, California, USA.
10
Department of Biological Sciences, University of Cape Town, Cape Town, South Africa.
11
Environmental Studies Department, University of California, Santa Cruz, Santa Cruz, California, USA.
12
Santa Monica Mountains National Recreation Area, National Park Service, Thousand Oaks, California, USA.
13
Department of Fish, Wildlife, and Conservation Biology, Graduate Degree Program in Ecology, Colorado State University, Fort Collins, Colorado, USA.
14
Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA sue.vandewoude@colostate.edu.

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.IMPORTANCE Cross-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.

KEYWORDS:

bobcat; cross-species transmission; feline; feline immunodeficiency virus; mountain lion; retroviruses

PMID:
28003486
PMCID:
PMC5309969
DOI:
10.1128/JVI.02134-16
[Indexed for MEDLINE]
Free PMC Article

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