Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada

Canine circoviruses (CanineCV) have a worldwide distribution in dogs and are occasionally detected in wild carnivorans, indicating their ability for cross-species transmission. However, fox circovirus, a lineage of CanineCV, has been identified exclusively in wild canids. We analyzed spleen samples...

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Main Authors: Canuti, Marta, King, Abigail V.L., Franzo, Giovanni, Cluff, H. Dean, Larsen, Lars E., Fenton, Heather, Dufour, Suzanne C., Lang, Andrew S.
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Language:English
Published: Peer Community In 2024-08-01
Series:Peer Community Journal
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Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.443/
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author Canuti, Marta
King, Abigail V.L.
Franzo, Giovanni
Cluff, H. Dean
Larsen, Lars E.
Fenton, Heather
Dufour, Suzanne C.
Lang, Andrew S.
author_facet Canuti, Marta
King, Abigail V.L.
Franzo, Giovanni
Cluff, H. Dean
Larsen, Lars E.
Fenton, Heather
Dufour, Suzanne C.
Lang, Andrew S.
author_sort Canuti, Marta
collection DOAJ
description Canine circoviruses (CanineCV) have a worldwide distribution in dogs and are occasionally detected in wild carnivorans, indicating their ability for cross-species transmission. However, fox circovirus, a lineage of CanineCV, has been identified exclusively in wild canids. We analyzed spleen samples from 159 grey wolves from the Northwest Territories, Canada, to investigate the molecular epidemiology of CanineCV and formulate hypotheses about virus ecology and evolution. Overall, 72 out of 159 (45.3%) animals tested positive. Virus prevalence was similar between males and females, adults and juveniles, and across the investigated years and locations. CanineCV infection was not associated with a poor body condition. While the percentage of co-infections with canine parvoviruses, investigated in a previous study, was high (63/72, 87.5%), the rate of parvovirus infection in CanineCV-negative animals was significantly lower (42/87, 48.3%, χ2 = 27.03, p < 0.001), and CanineCV infection was associated with a 7.5- and 2.4-fold increase in the risk of acquiring canine parvovirus 2 or canine bufavirus infections, respectively (odds ratios: 3.5-16.9 and 1.3-5.8). Although common risk factors cannot be ruled out, this suggests that CanineCV may facilitate parvoviral super-infections. Sequencing revealed high CanineCV genetic diversity, further exacerbated by recombination. Of the 69 sequenced strains, 87.5% were fox circoviruses, five were related to a fox circovirus-like recombinant strain, and one belonged to a distant lineage. In the phylogenetic analysis, the virus sequences were distributed according to sampling locations, with some viruses being geographically restricted. Different clades of viruses were identified in the same areas and over multiple years (2007-2019), indicating the co-existence of multiple endemic lineages in the investigated area. Phylogenetic analysis of all available complete fox circovirus genomes (32 from foxes and 15 from wolves from North America and Europe) demonstrated four lineages, each including sequences from this study. Within each lineage, strains segregated geographically and not by host. This implies that, although multiple lineages co-exist, viruses do not frequently move between locations. Finally, viruses from Europe and North America were mixed, indicating that the origin of the four lineages might predate the segregation of European and American wolf and fox populations. Given the high prevalence and diversity of fox circoviruses in wolves, these animals should be considered reservoir hosts for these viruses. Although we cannot exclude a lower susceptibility of dogs, the lack of fox circovirus in dogs could be due to environmental circumstances that prevented its spread to dogs. Given the high diversity and wild host specificity, we presume a long-lasting association between fox circovirus and canine hosts and hypothesize a higher likelihood of transmission from dogs to wild animals than vice versa. Further studies should investigate other sympatric wild species and additional locations to explore the possible existence of additional maintenance hosts and the reasons behind the marked difference in cross-species transmission dynamics among CanineCV lineages.
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spelling doaj-art-536f02e3a7f44fb184ab2f6777000c632025-02-07T10:17:18ZengPeer Community InPeer Community Journal2804-38712024-08-01410.24072/pcjournal.44310.24072/pcjournal.443Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada Canuti, Marta0https://orcid.org/0000-0002-9959-128XKing, Abigail V.L.1Franzo, Giovanni2https://orcid.org/0000-0003-2991-217XCluff, H. Dean3https://orcid.org/0000-0002-9233-1450Larsen, Lars E.4https://orcid.org/0000-0003-0730-5555Fenton, Heather5https://orcid.org/0000-0002-0190-8921Dufour, Suzanne C.6Lang, Andrew S.7https://orcid.org/0000-0002-4510-7683Department of Veterinary and Animal Sciences, University of Copenhagen, Frederiksberg, 1870, DenmarkDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, CanadaDepartment of Animal Medicine, Production and Health (MAPS), Padua University, 35020, Legnaro, ItalyEnvironment and Climate Change – North Slave Region, Government of the Northwest Territories, Yellowknife, NT X1A 2P9, CanadaDepartment of Veterinary and Animal Sciences, University of Copenhagen, Frederiksberg, 1870, DenmarkEnvironment and Climate Change – North Slave Region, Government of the Northwest Territories, Yellowknife, NT X1A 2P9, CanadaDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, CanadaDepartment of Biology, Memorial University of Newfoundland, St. John’s, NL A1C 5S7, CanadaCanine circoviruses (CanineCV) have a worldwide distribution in dogs and are occasionally detected in wild carnivorans, indicating their ability for cross-species transmission. However, fox circovirus, a lineage of CanineCV, has been identified exclusively in wild canids. We analyzed spleen samples from 159 grey wolves from the Northwest Territories, Canada, to investigate the molecular epidemiology of CanineCV and formulate hypotheses about virus ecology and evolution. Overall, 72 out of 159 (45.3%) animals tested positive. Virus prevalence was similar between males and females, adults and juveniles, and across the investigated years and locations. CanineCV infection was not associated with a poor body condition. While the percentage of co-infections with canine parvoviruses, investigated in a previous study, was high (63/72, 87.5%), the rate of parvovirus infection in CanineCV-negative animals was significantly lower (42/87, 48.3%, χ2 = 27.03, p < 0.001), and CanineCV infection was associated with a 7.5- and 2.4-fold increase in the risk of acquiring canine parvovirus 2 or canine bufavirus infections, respectively (odds ratios: 3.5-16.9 and 1.3-5.8). Although common risk factors cannot be ruled out, this suggests that CanineCV may facilitate parvoviral super-infections. Sequencing revealed high CanineCV genetic diversity, further exacerbated by recombination. Of the 69 sequenced strains, 87.5% were fox circoviruses, five were related to a fox circovirus-like recombinant strain, and one belonged to a distant lineage. In the phylogenetic analysis, the virus sequences were distributed according to sampling locations, with some viruses being geographically restricted. Different clades of viruses were identified in the same areas and over multiple years (2007-2019), indicating the co-existence of multiple endemic lineages in the investigated area. Phylogenetic analysis of all available complete fox circovirus genomes (32 from foxes and 15 from wolves from North America and Europe) demonstrated four lineages, each including sequences from this study. Within each lineage, strains segregated geographically and not by host. This implies that, although multiple lineages co-exist, viruses do not frequently move between locations. Finally, viruses from Europe and North America were mixed, indicating that the origin of the four lineages might predate the segregation of European and American wolf and fox populations. Given the high prevalence and diversity of fox circoviruses in wolves, these animals should be considered reservoir hosts for these viruses. Although we cannot exclude a lower susceptibility of dogs, the lack of fox circovirus in dogs could be due to environmental circumstances that prevented its spread to dogs. Given the high diversity and wild host specificity, we presume a long-lasting association between fox circovirus and canine hosts and hypothesize a higher likelihood of transmission from dogs to wild animals than vice versa. Further studies should investigate other sympatric wild species and additional locations to explore the possible existence of additional maintenance hosts and the reasons behind the marked difference in cross-species transmission dynamics among CanineCV lineages.https://peercommunityjournal.org/articles/10.24072/pcjournal.443/circovirus; wildlife; canine viruses; virus ecology;
spellingShingle Canuti, Marta
King, Abigail V.L.
Franzo, Giovanni
Cluff, H. Dean
Larsen, Lars E.
Fenton, Heather
Dufour, Suzanne C.
Lang, Andrew S.
Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
Peer Community Journal
circovirus; wildlife; canine viruses; virus ecology;
title Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
title_full Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
title_fullStr Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
title_full_unstemmed Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
title_short Diverse fox circovirus (Circovirus canine) variants circulate at high prevalence in grey wolves (Canis lupus) from the Northwest Territories, Canada
title_sort diverse fox circovirus circovirus canine variants circulate at high prevalence in grey wolves canis lupus from the northwest territories canada
topic circovirus; wildlife; canine viruses; virus ecology;
url https://peercommunityjournal.org/articles/10.24072/pcjournal.443/
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