title: Evolution of puma lentivirus in bobcats (Lynx rufus) and mountain lions (Puma concolor) in North America.
abstract: Mountain lions (Puma concolor) throughout North and South America are infected with puma lentivirus clade B (PLVB). A second, highly divergent lentiviral clade, PLVA, infects mountain lions in southern California and Florida. Bobcats (Lynx rufus) in these two geographic regions are also infected with PLVA, and to date, this is the only strain of lentivirus identified in bobcats. We sequenced full-length PLV genomes in order to characterize the molecular evolution of PLV in bobcats and mountain lions. Low sequence homology (88% average pairwise identity) and frequent recombination (1 recombination breakpoint per 3 isolates analyzed) were observed in both clades. Viral proteins have markedly different patterns of evolution; sequence homology and negative selection were highest in Gag and Pol and lowest in Vif and Env. A total of 1.7% of sites across the PLV genome evolve under positive selection, indicating that host-imposed selection pressure is an important force shaping PLV evolution. PLVA strains are highly spatially structured, reflecting the population dynamics of their primary host, the bobcat. In contrast, the phylogeography of PLVB reflects the highly mobile mountain lion, with diverse PLVB isolates cocirculating in some areas and genetically related viruses being present in populations separated by thousands of kilometers. We conclude that PLVA and PLVB are two different viral species with distinct feline hosts and evolutionary histories. Importance: An understanding of viral evolution in natural host populations is a fundamental goal of virology, molecular biology, and disease ecology. Here we provide a detailed analysis of puma lentivirus (PLV) evolution in two natural carnivore hosts, the bobcat and mountain lion. Our results illustrate that PLV evolution is a dynamic process that results from high rates of viral mutation/recombination and host-imposed selection pressure.
authors.affiliation: Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado, USA justinlee337@gmail.com.
authors.forename: Justin S
authors.initials: JS
authors.lastname: Lee
authors.affiliation: USDA National Wildlife Research Center, Fort Collins, Colorado, USA.
authors.forename: Sarah N
authors.initials: SN
authors.lastname: Bevins
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California-Los Angeles, Los Angeles, California, USA.
authors.forename: Laurel E K
authors.initials: LE
authors.lastname: Serieys
authors.affiliation: Department of Pathology, Microbiology, and Immunology, University of California-Davis, Davis, California, USA.
authors.forename: Winston
authors.initials: W
authors.lastname: Vickers
authors.affiliation: Colorado Parks and Wildlife, Montrose, Colorado, USA.
authors.forename: Ken A
authors.initials: KA
authors.lastname: Logan
authors.affiliation: Colorado Parks and Wildlife, Fort Collins, Colorado, USA.
authors.forename: Mat
authors.initials: M
authors.lastname: Aldredge
authors.affiliation: USGS Western Ecological Research Center, Thousand Oaks, California, USA.
authors.forename: Erin E
authors.initials: EE
authors.lastname: Boydston
authors.affiliation: USGS Western Ecological Research Center, Thousand Oaks, California, USA.
authors.forename: Lisa M
authors.initials: LM
authors.lastname: Lyren
authors.affiliation: Rancher's Supply Inc., Ochopee, Florida, USA.
authors.forename: Roy
authors.initials: R
authors.lastname: McBride
authors.affiliation: Laboratory of Genetic Diversity, National Cancer Institute, Frederick, Maryland, USA.
authors.forename: Melody
authors.initials: M
authors.lastname: Roelke-Parker
authors.affiliation: Laboratory of Genetic Diversity, National Cancer Institute, Frederick, Maryland, USA.
authors.forename: Jill
authors.initials: J
authors.lastname: Pecon-Slattery
authors.affiliation: Laboratory of Genetic Diversity, National Cancer Institute, Frederick, Maryland, USA.
authors.forename: Jennifer L
authors.initials: JL
authors.lastname: Troyer
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California-Los Angeles, Los Angeles, California, USA.
authors.forename: Seth P
authors.initials: SP
authors.lastname: Riley
authors.affiliation: Department of Pathology, Microbiology, and Immunology, University of California-Davis, Davis, California, USA.
authors.forename: Walter M
authors.initials: WM
authors.lastname: Boyce
authors.affiliation: Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Crooks
authors.affiliation: Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado, USA.
authors.forename: Sue
authors.initials: S
authors.lastname: VandeWoude
mesh_terms: D000818:Animals; D016000:Cluster Analysis; D019143:Evolution, Molecular; D014644:Genetic Variation; D016679:Genome, Viral; D016089:Immunodeficiency Virus, Feline / Q000145:classification / Q000235:genetics / Q000302:isolation & purification*; D046008:Lynx / Q000821:virology*; D008969:Molecular Sequence Data; D009656:North America; D058974:Phylogeography; D046011:Puma / Q000821:virology*; D012367:RNA, Viral / Q000235:genetics*; D011995:Recombination, Genetic; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D014764:Viral Proteins / Q000235:genetics
chemical_list: D012367:RNA, Viral; D014764:Viral Proteins
references.citation: Virus Genes. 2007 Oct;35(2):251-64
references.pmid: 17265140
references.citation: J Virol. 2005 Jul;79(13):8282-94
references.pmid: 15956574
references.citation: Mol Ecol. 2012 Jun;21(12):3078-93
references.pmid: 22548482
references.citation: Mol Biol Evol. 2011 Nov;28(11):3033-43
references.pmid: 21670087
references.citation: Virology. 1987 Dec;161(2):321-31
references.pmid: 2825406
references.citation: Vet Immunol Immunopathol. 2010 Mar 15;134(1-2):25-32
references.pmid: 19896218
references.citation: Cell. 2003 Jul 11;114(1):21-31
references.pmid: 12859895
references.citation: Mol Biol Evol. 2005 May;22(5):1185-92
references.pmid: 15703244
references.citation: Virology. 1994 Aug 1;202(2):853-64
references.pmid: 8030248
references.citation: Vet Immunol Immunopathol. 2010 Mar 15;134(1-2):3-13
references.pmid: 19910057
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147
references.citation: Nat Med. 1999 Nov;5(11):1270-6
references.pmid: 10545993
references.citation: J Virol. 1987 Dec;61(12):4046-54
references.pmid: 2824836
references.citation: Virology. 2001 Jan 5;279(1):185-200
references.pmid: 11145901
references.citation: Mol Biol Evol. 2001 Oct;18(10):1929-39
references.pmid: 11557798
references.citation: J Virol. 2002 Oct;76(19):9624-34
references.pmid: 12208941
references.citation: Nucleic Acids Res. 2011 Jan;39(Database issue):D32-7
references.pmid: 21071399
references.citation: Nucleic Acids Res. 2007 Jul;35(Web Server issue):W43-6
references.pmid: 17452344
references.citation: Mol Ecol. 2012 Apr;21(7):1617-31
references.pmid: 22335296
references.citation: Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4835-9
references.pmid: 1594583
references.citation: Biol Conserv. 2006 Aug;131(2):255-267
references.pmid: 32226081
references.citation: Clin Microbiol Rev. 2006 Oct;19(4):728-62
references.pmid: 17041142
references.citation: J Virol. 2006 Mar;80(6):2728-37
references.pmid: 16501082
references.citation: Bioinformatics. 2010 Oct 1;26(19):2455-7
references.pmid: 20671151
references.citation: J Virol. 1996 Oct;70(10):6682-93
references.pmid: 8794304
references.citation: Virology. 2008 Jan 5;370(1):55-62
references.pmid: 17904608
references.citation: J Virol. 1992 Sep;66(9):5464-71
references.pmid: 1323707
references.citation: Mol Biol Evol. 2005 May;22(5):1208-22
references.pmid: 15703242
references.citation: J Virol. 2010 Jul;84(14):7312-24
references.pmid: 20444897
references.citation: Vet Immunol Immunopathol. 2008 May 15;123(1-2):32-44
references.pmid: 18359092
references.citation: PLoS One. 2012;7(2):e31403
references.pmid: 22347471
references.citation: Mol Biol Evol. 2006 Oct;23(10):1891-901
references.pmid: 16818476
references.citation: Virology. 2007 Aug 1;364(2):362-70
references.pmid: 17445856
references.citation: J Virol. 1993 Apr;67(4):1869-76
references.pmid: 8383214
references.citation: BMC Evol Biol. 2007 Nov 08;7:214
references.pmid: 17996036
references.citation: J Virol. 2007 Oct;81(20):10961-9
references.pmid: 17670835
references.citation: J Hered. 2000 May-Jun;91(3):186-97
references.pmid: 10833043
references.citation: Curr Biol. 2004 Aug 10;14(15):1392-6
references.pmid: 15296758
references.citation: J Virol. 2002 Nov;76(22):11715-20
references.pmid: 12388731
references.citation: Mol Ecol. 2006 Jun;15(7):1733-41
references.pmid: 16689893
references.citation: Conserv Genet. 2003;4(3):353-366
references.pmid: 32214916
references.citation: J Wildl Dis. 2013 Jul;49(3):718-22
references.pmid: 23778629
references.citation: J Gen Virol. 1993 Mar;74 ( Pt 3):425-36
references.pmid: 8383177
references.citation: BMC Genomics. 2008 Feb 05;9:66
references.pmid: 18251995
references.citation: J Virol. 1999 Sep;73(9):7916-21
references.pmid: 10438892
references.citation: J Virol. 2003 Sep;77(17):9578-89
references.pmid: 12915571
references.citation: Nature. 1989 Mar 16;338(6212):254-7
references.pmid: 2784194
references.citation: J Virol. 1992 Oct;66(10):6008-18
references.pmid: 1382145