A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population

Abstract The identification of a new circovirus (Porcine circovirus 3, PCV‐3) has raised a remarkable concern because of some analogies with Porcine circovirus 2 (PCV‐2). Preliminary results suggest an extremely recent PCV‐3 emergence and high mutation rate. Retrospective studies prove its circulati...

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Main Authors: Giovanni Franzo, Wanting He, Florencia Correa‐Fiz, Gairu Li, Matteo Legnardi, Shuo Su, Joaquim Segalés
Format: Article
Language:English
Published: Wiley 2019-11-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.201901004
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spelling doaj-8093775179d64b8db6c7fd594e4535b32020-11-25T01:50:24ZengWileyAdvanced Science2198-38442019-11-01622n/an/a10.1002/advs.201901004A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine PopulationGiovanni Franzo0Wanting He1Florencia Correa‐Fiz2Gairu Li3Matteo Legnardi4Shuo Su5Joaquim Segalés6Department of Animal Medicine Production and Health (MAPS) University of Padua Viale, dell'Università 16 35020 Legnaro (PD) ItalyMOE International Joint Collaborative Research Laboratory for Animal Health & Food Safety Jiangsu Engineering Laboratory of Animal Immunology Institute of Immunology College of Veterinary Medicine Nanjing Agricultural University Nanjing 210000 ChinaIRTA Centre de Recerca en Sanitat Animal (CReSA, IRTA‐UAB) Campus de la Universitat Autònoma de Barcelona Bellaterra 08913 SpainMOE International Joint Collaborative Research Laboratory for Animal Health & Food Safety Jiangsu Engineering Laboratory of Animal Immunology Institute of Immunology College of Veterinary Medicine Nanjing Agricultural University Nanjing 210000 ChinaDepartment of Animal Medicine Production and Health (MAPS) University of Padua Viale, dell'Università 16 35020 Legnaro (PD) ItalyMOE International Joint Collaborative Research Laboratory for Animal Health & Food Safety Jiangsu Engineering Laboratory of Animal Immunology Institute of Immunology College of Veterinary Medicine Nanjing Agricultural University Nanjing 210000 ChinaUAB Centre de Recerca en Sanitat Animal (CReSA, IRTA‐UAB) Campus de la Universitat Autònoma de Barcelona Bellaterra 08913 SpainAbstract The identification of a new circovirus (Porcine circovirus 3, PCV‐3) has raised a remarkable concern because of some analogies with Porcine circovirus 2 (PCV‐2). Preliminary results suggest an extremely recent PCV‐3 emergence and high mutation rate. Retrospective studies prove its circulation at least since the early 1990s, revealing that PCV‐3 could have been infecting pigs for an even longer period. Therefore, a new evaluation, based on an updated collection of PCV‐3 sequences spanning more than 20 years, is performed using a phylodynamic approach. The obtained results overrule the previous PCV‐3 history concept, indicating an ancient origin. These evidences are associated with an evolutionary rate far lower (10−5–10−6 substitution/site/year) than the PCV‐2 one. Accordingly, the action of selective pressures on PCV‐3 open reading frames (ORFs) seems to be remarkably lower compared to those acting on PCV‐2, suggesting either a reduced PCV‐3 plasticity or a less efficient host‐induced natural selection. A complex and not‐directional viral flow network is evidenced through phylogeographic analysis, indicating a long lasting circulation rather than a recent emergence followed by spreading. Being recent emergence has been ruled out, efforts should be devoted to understand whether its recent discovery is simply due to improved detection capabilities or to the breaking of a previous equilibrium.https://doi.org/10.1002/advs.201901004epidemiologyevolutionporcine circovirus 3 (PCV‐3)phylodynamicphylogeography
collection DOAJ
language English
format Article
sources DOAJ
author Giovanni Franzo
Wanting He
Florencia Correa‐Fiz
Gairu Li
Matteo Legnardi
Shuo Su
Joaquim Segalés
spellingShingle Giovanni Franzo
Wanting He
Florencia Correa‐Fiz
Gairu Li
Matteo Legnardi
Shuo Su
Joaquim Segalés
A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
Advanced Science
epidemiology
evolution
porcine circovirus 3 (PCV‐3)
phylodynamic
phylogeography
author_facet Giovanni Franzo
Wanting He
Florencia Correa‐Fiz
Gairu Li
Matteo Legnardi
Shuo Su
Joaquim Segalés
author_sort Giovanni Franzo
title A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
title_short A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
title_full A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
title_fullStr A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
title_full_unstemmed A Shift in Porcine Circovirus 3 (PCV‐3) History Paradigm: Phylodynamic Analyses Reveal an Ancient Origin and Prolonged Undetected Circulation in the Worldwide Swine Population
title_sort shift in porcine circovirus 3 (pcv‐3) history paradigm: phylodynamic analyses reveal an ancient origin and prolonged undetected circulation in the worldwide swine population
publisher Wiley
series Advanced Science
issn 2198-3844
publishDate 2019-11-01
description Abstract The identification of a new circovirus (Porcine circovirus 3, PCV‐3) has raised a remarkable concern because of some analogies with Porcine circovirus 2 (PCV‐2). Preliminary results suggest an extremely recent PCV‐3 emergence and high mutation rate. Retrospective studies prove its circulation at least since the early 1990s, revealing that PCV‐3 could have been infecting pigs for an even longer period. Therefore, a new evaluation, based on an updated collection of PCV‐3 sequences spanning more than 20 years, is performed using a phylodynamic approach. The obtained results overrule the previous PCV‐3 history concept, indicating an ancient origin. These evidences are associated with an evolutionary rate far lower (10−5–10−6 substitution/site/year) than the PCV‐2 one. Accordingly, the action of selective pressures on PCV‐3 open reading frames (ORFs) seems to be remarkably lower compared to those acting on PCV‐2, suggesting either a reduced PCV‐3 plasticity or a less efficient host‐induced natural selection. A complex and not‐directional viral flow network is evidenced through phylogeographic analysis, indicating a long lasting circulation rather than a recent emergence followed by spreading. Being recent emergence has been ruled out, efforts should be devoted to understand whether its recent discovery is simply due to improved detection capabilities or to the breaking of a previous equilibrium.
topic epidemiology
evolution
porcine circovirus 3 (PCV‐3)
phylodynamic
phylogeography
url https://doi.org/10.1002/advs.201901004
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