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Emergence of Pathogenicity in Lagoviruses: Evolution from Pre-existing Nonpathogenic Strains or through a Species Jump?

Esteves PJ, Abrantes J, Bertagnoli S, Cavadini P, Gavier-Widén D, Guitton JS, Lavazza A, Lemaitre E, Letty J, Lopes AM, Neimanis AS, Ruvoën-Clouet N, Le Pendu J, Marchandeau S, Le Gall-Reculé G - PLoS Pathog. (2015)

View Article: PubMed Central - PubMed

Affiliation: InBIO-Research Network in Biodiversity and Evolutionary Biology, CIBIO, Campus de Vairão, Universidade do Porto, Vairão, Portugal.

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Both cause high mortalities and impose a heavy economic burden on the rabbit industry and game animal management... They have also contributed to declines of wild leporid populations throughout Europe, resulting in major ecological impact in natural ecosystems where leporids are key species... Rabbit lagoviruses consist of pathogenic viruses (RHDV) and related, but genetically divergent, nonpathogenic viruses... RHDV2 was identified in France and has since spread throughout other Western European countries, replacing the circulating strains in France and the Iberian Peninsula, while in Italy, it currently cocirculates with the “original” strains... EBHS was first reported in Sweden in 1980 and later found in other European countries... Two competing hypotheses can be put forward to explain RHDV and EBHSV origin and the emergence of RHDV2: 1) the evolution from pre-existing nonpathogenic viruses circulating in European leporids; 2) a species jump... Notably, the pathogenic and nonpathogenic viruses are phylogenetically separated and display ~20% of nucleotide divergence in the capsid gene, suggesting that the pathogenic forms did not directly originate from the nonpathogenic ones... Nevertheless, nonpathogenic strains have not been exhaustively characterized in European leporids, which may explain why the ancestors of pathogenic strains have not yet been found... Moreover, recent documentation of RHDV strains in Iberian hares (L. granatensis) with lesions compatible with RHD, demonstration of the capacity of RHDV2 to infect Sardinian Cape and Italian hares (L. capensis mediterraneus and L. corsicanus, respectively) causing RHDV-like disease, and the experimental infection of cottontails by EBHSV, show the feasibility of species jumps of lagoviruses between leporid species... We therefore suggest that European leporids carry lagoviruses of two distinct origins (Fig 1): nonpathogenic strains that have evolved with these species for a long time and a second group including pathogenic strains that possibly emerged following species jumps from S. floridanus and that have then evolved in European leporids... Pathogenic strains may be pure cottontail viruses or recombinants of cottontail viruses and nonpathogenic viruses of European leporid species... Indeed, recombination in RHDV is reported, and the recent documentation of recombination events between genome regions encoding the capsid and VP10 structural proteins of RHDV2 and the nonstructural proteins from nonpathogenic or pathogenic G1 lagoviruses suggests that recombination could have had an important role in the lagovirus evolution... Evaluation of potential emergence of new pathogenic lagoviruses from the nonpathogenic strains circulating among native European leporid species and Sylvilagus species, as well as characterization of the genetic determinisms of pathogenicity, are key to identify the mechanisms of disease emergence and may help to evaluate the possibility of emergence of other highly pathogenic lagoviruses.

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Possible origin of European rabbit (O. cuniculus) lagoviruses according to the hypothesis of a species jump.A) Lagoviruses that may share common ancestors following several species jump(s), B) Nonpathogenic viruses that have evolved in European rabbit for a long time. Phylogenetic tree (Neighbor-joining method) derived from 303 rabbit lagovirus sequences of the VP60 gene available on public databases (May 2015). The pathogenic RHDV, RHDVa, RHDV2, and the nonpathogenic RCV-A1 branches are collapsed; the name of the leporid species where these strains were isolated is given in brackets. X96868_RCV/1996-Italy, GQ166866_MRCV/2000-USA, EF558587_Ashington/1998-UK, and AM268419_06-11/2006-France are nonpathogenic strains isolated in the European rabbit. Percentage greater than 70% of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are given at major branch nodes. The EBHSV strain GD (Z69620) was used as an outgroup to root the tree. Similar clustering was observed in several recent works [63,64,66,70,74].
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ppat.1005087.g001: Possible origin of European rabbit (O. cuniculus) lagoviruses according to the hypothesis of a species jump.A) Lagoviruses that may share common ancestors following several species jump(s), B) Nonpathogenic viruses that have evolved in European rabbit for a long time. Phylogenetic tree (Neighbor-joining method) derived from 303 rabbit lagovirus sequences of the VP60 gene available on public databases (May 2015). The pathogenic RHDV, RHDVa, RHDV2, and the nonpathogenic RCV-A1 branches are collapsed; the name of the leporid species where these strains were isolated is given in brackets. X96868_RCV/1996-Italy, GQ166866_MRCV/2000-USA, EF558587_Ashington/1998-UK, and AM268419_06-11/2006-France are nonpathogenic strains isolated in the European rabbit. Percentage greater than 70% of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are given at major branch nodes. The EBHSV strain GD (Z69620) was used as an outgroup to root the tree. Similar clustering was observed in several recent works [63,64,66,70,74].

Mentions: We therefore suggest that European leporids carry lagoviruses of two distinct origins (Fig 1): nonpathogenic strains that have evolved with these species for a long time and a second group including pathogenic strains that possibly emerged following species jumps from S. floridanus and that have then evolved in European leporids. Pathogenic strains may be pure cottontail viruses or recombinants of cottontail viruses and nonpathogenic viruses of European leporid species. Indeed, recombination in RHDV is reported [96,97], and the recent documentation of recombination events between genome regions encoding the capsid and VP10 structural proteins of RHDV2 and the nonstructural proteins from nonpathogenic or pathogenic G1 lagoviruses suggests that recombination could have had an important role in the lagovirus evolution [74].


Emergence of Pathogenicity in Lagoviruses: Evolution from Pre-existing Nonpathogenic Strains or through a Species Jump?

Esteves PJ, Abrantes J, Bertagnoli S, Cavadini P, Gavier-Widén D, Guitton JS, Lavazza A, Lemaitre E, Letty J, Lopes AM, Neimanis AS, Ruvoën-Clouet N, Le Pendu J, Marchandeau S, Le Gall-Reculé G - PLoS Pathog. (2015)

Possible origin of European rabbit (O. cuniculus) lagoviruses according to the hypothesis of a species jump.A) Lagoviruses that may share common ancestors following several species jump(s), B) Nonpathogenic viruses that have evolved in European rabbit for a long time. Phylogenetic tree (Neighbor-joining method) derived from 303 rabbit lagovirus sequences of the VP60 gene available on public databases (May 2015). The pathogenic RHDV, RHDVa, RHDV2, and the nonpathogenic RCV-A1 branches are collapsed; the name of the leporid species where these strains were isolated is given in brackets. X96868_RCV/1996-Italy, GQ166866_MRCV/2000-USA, EF558587_Ashington/1998-UK, and AM268419_06-11/2006-France are nonpathogenic strains isolated in the European rabbit. Percentage greater than 70% of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are given at major branch nodes. The EBHSV strain GD (Z69620) was used as an outgroup to root the tree. Similar clustering was observed in several recent works [63,64,66,70,74].
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4634945&req=5

ppat.1005087.g001: Possible origin of European rabbit (O. cuniculus) lagoviruses according to the hypothesis of a species jump.A) Lagoviruses that may share common ancestors following several species jump(s), B) Nonpathogenic viruses that have evolved in European rabbit for a long time. Phylogenetic tree (Neighbor-joining method) derived from 303 rabbit lagovirus sequences of the VP60 gene available on public databases (May 2015). The pathogenic RHDV, RHDVa, RHDV2, and the nonpathogenic RCV-A1 branches are collapsed; the name of the leporid species where these strains were isolated is given in brackets. X96868_RCV/1996-Italy, GQ166866_MRCV/2000-USA, EF558587_Ashington/1998-UK, and AM268419_06-11/2006-France are nonpathogenic strains isolated in the European rabbit. Percentage greater than 70% of replicate trees in which the associated taxa clustered together in the bootstrap test (500 replicates) are given at major branch nodes. The EBHSV strain GD (Z69620) was used as an outgroup to root the tree. Similar clustering was observed in several recent works [63,64,66,70,74].
Mentions: We therefore suggest that European leporids carry lagoviruses of two distinct origins (Fig 1): nonpathogenic strains that have evolved with these species for a long time and a second group including pathogenic strains that possibly emerged following species jumps from S. floridanus and that have then evolved in European leporids. Pathogenic strains may be pure cottontail viruses or recombinants of cottontail viruses and nonpathogenic viruses of European leporid species. Indeed, recombination in RHDV is reported [96,97], and the recent documentation of recombination events between genome regions encoding the capsid and VP10 structural proteins of RHDV2 and the nonstructural proteins from nonpathogenic or pathogenic G1 lagoviruses suggests that recombination could have had an important role in the lagovirus evolution [74].

View Article: PubMed Central - PubMed

Affiliation: InBIO-Research Network in Biodiversity and Evolutionary Biology, CIBIO, Campus de Vairão, Universidade do Porto, Vairão, Portugal.

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

Both cause high mortalities and impose a heavy economic burden on the rabbit industry and game animal management... They have also contributed to declines of wild leporid populations throughout Europe, resulting in major ecological impact in natural ecosystems where leporids are key species... Rabbit lagoviruses consist of pathogenic viruses (RHDV) and related, but genetically divergent, nonpathogenic viruses... RHDV2 was identified in France and has since spread throughout other Western European countries, replacing the circulating strains in France and the Iberian Peninsula, while in Italy, it currently cocirculates with the “original” strains... EBHS was first reported in Sweden in 1980 and later found in other European countries... Two competing hypotheses can be put forward to explain RHDV and EBHSV origin and the emergence of RHDV2: 1) the evolution from pre-existing nonpathogenic viruses circulating in European leporids; 2) a species jump... Notably, the pathogenic and nonpathogenic viruses are phylogenetically separated and display ~20% of nucleotide divergence in the capsid gene, suggesting that the pathogenic forms did not directly originate from the nonpathogenic ones... Nevertheless, nonpathogenic strains have not been exhaustively characterized in European leporids, which may explain why the ancestors of pathogenic strains have not yet been found... Moreover, recent documentation of RHDV strains in Iberian hares (L. granatensis) with lesions compatible with RHD, demonstration of the capacity of RHDV2 to infect Sardinian Cape and Italian hares (L. capensis mediterraneus and L. corsicanus, respectively) causing RHDV-like disease, and the experimental infection of cottontails by EBHSV, show the feasibility of species jumps of lagoviruses between leporid species... We therefore suggest that European leporids carry lagoviruses of two distinct origins (Fig 1): nonpathogenic strains that have evolved with these species for a long time and a second group including pathogenic strains that possibly emerged following species jumps from S. floridanus and that have then evolved in European leporids... Pathogenic strains may be pure cottontail viruses or recombinants of cottontail viruses and nonpathogenic viruses of European leporid species... Indeed, recombination in RHDV is reported, and the recent documentation of recombination events between genome regions encoding the capsid and VP10 structural proteins of RHDV2 and the nonstructural proteins from nonpathogenic or pathogenic G1 lagoviruses suggests that recombination could have had an important role in the lagovirus evolution... Evaluation of potential emergence of new pathogenic lagoviruses from the nonpathogenic strains circulating among native European leporid species and Sylvilagus species, as well as characterization of the genetic determinisms of pathogenicity, are key to identify the mechanisms of disease emergence and may help to evaluate the possibility of emergence of other highly pathogenic lagoviruses.

No MeSH data available.


Related in: MedlinePlus