The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights

Autores
Schnittger, Leonhard; Ganzinelli, Sabrina Belen; Bhoora, Raksha; Omondi, David; Nijhof, Ard M.; Florin-Christensen, Mónica
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The order Piroplasmida, including the genera Babesia, Cytauxzoon, and Theileria is often referred to as piroplasmids and comprises of dixenous hemoprotozoans transmitted by ticks to a mammalian or avian host. Although piroplasmid infections are usually asymptomatic in wild animals, in domestic animals, they cause serious or life-threatening consequences resulting in fatalities. Piroplasmids are particularly notorious for the enormous economic loss they cause worldwide in livestock production, the restrictions they pose on horse trade, and the negative health impact they have on dogs and cats. Furthermore, an increasing number of reported human babesiosis cases are of growing concern. Considerable international research and epidemiological studies are done to identify existing parasite species, reveal their phylogenetic relationships, and develop improved or new drugs and vaccines to mitigate their impact. In this review, we present a compilation of all piroplasmid species, isolates, and species complexes that infect domestic mammals and which have been well defined by molecular phylogenetic markers. Altogether, 57 taxonomic piroplasmid entities were compiled, comprising of 43 piroplasmid species, 12 well-defined isolates awaiting formal species description, and two species complexes that possibly mask additional species. The extrapolation of the finding of at least 57 piroplasmid species in only six domestic mammalian groups (cattle, sheep, goat, horse, dog, and cat) allows us to predict that a substantially higher number of piroplasmid parasites than vertebrate host species exist. Accordingly, the infection of a vertebrate host species by multiple piroplasmid species from the same and/or different phylogenetic lineages is commonly observed. Molecular phylogeny using 18S rRNA genes of piroplasmids infecting domestic mammals results in the formation of six clades, which emerge due to an anthropocentric research scope, but not due to a possibly assumed biological priority position. Scrutinizing the topology of inferred trees reveals stunning insights into some evolutionary patterns exhibited by this intriguing group of parasites. Contrary to expectations, diversification of parasite species appears to be dominated by host-parasite cospeciation (Fahrenholz’s rule), and, except for piroplasmids that segregate into Clade VI, host switching is rarely observed. When only domestic mammalian hosts are taken into account, Babesia sensu lato (s.l.) parasites of Clades I and II infect only dogs and cats, respectively, Cytauxzoon spp. placed into Clade III only infect cats, Theileria placed into Clade IV exclusively infect horses, wheras Theileria sensu stricto (s.s.) of Clade V infects only cattle and small ruminants. In contrast, Babesia s.s. parasites of Clade VI infect all farm and companion animal species. We outline how the unique ability of transovarial transmission of Babesia s.s. piroplasmids of Clade VI facilitates species diversification by host switching to other host vertebrate species. Finally, a deterioration of sequence fidelity in databases is observed which will likely lead to an increased risk of artifactual research in this area. Possible measures to reverse and/or avoid this threat are discussed.
Instituto de Patobiología
Fil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ganzinelli Sabrina Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Ganzinelli Sabrina Belen. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Bhoora, Raksha. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases; Sudáfrica
Fil: Omondi, David. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; Alemania
Fil: Omondi, David. Egerton University Njoro Campus. Department of Biochemistry and Molecular Biology; Kenia
Fil: Nijhof, Ard M. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; Alemania
Fil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
Parasitology Research 121 (5) : 1207-1245 (May 2022)
Materia
Phylogeny
Piroplasmea
Cattle
Sheep
Dogs
Cats
Goats
Horses
Evolution
Filogenia
Piroplásmea
Ganado Bovino
Ovinos
Perro
Gato
Caprinos
Caballos
Babesia
Cytauxzoon
Theileria
Evolución
Nivel de accesibilidad
acceso restringido
Condiciones de uso
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
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spelling The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insightsSchnittger, LeonhardGanzinelli, Sabrina BelenBhoora, RakshaOmondi, DavidNijhof, Ard M.Florin-Christensen, MónicaPhylogenyPiroplasmeaCattleSheepDogsCatsGoatsHorsesEvolutionFilogeniaPiroplásmeaGanado BovinoOvinosPerroGatoCaprinosCaballosBabesiaCytauxzoonTheileriaEvoluciónThe order Piroplasmida, including the genera Babesia, Cytauxzoon, and Theileria is often referred to as piroplasmids and comprises of dixenous hemoprotozoans transmitted by ticks to a mammalian or avian host. Although piroplasmid infections are usually asymptomatic in wild animals, in domestic animals, they cause serious or life-threatening consequences resulting in fatalities. Piroplasmids are particularly notorious for the enormous economic loss they cause worldwide in livestock production, the restrictions they pose on horse trade, and the negative health impact they have on dogs and cats. Furthermore, an increasing number of reported human babesiosis cases are of growing concern. Considerable international research and epidemiological studies are done to identify existing parasite species, reveal their phylogenetic relationships, and develop improved or new drugs and vaccines to mitigate their impact. In this review, we present a compilation of all piroplasmid species, isolates, and species complexes that infect domestic mammals and which have been well defined by molecular phylogenetic markers. Altogether, 57 taxonomic piroplasmid entities were compiled, comprising of 43 piroplasmid species, 12 well-defined isolates awaiting formal species description, and two species complexes that possibly mask additional species. The extrapolation of the finding of at least 57 piroplasmid species in only six domestic mammalian groups (cattle, sheep, goat, horse, dog, and cat) allows us to predict that a substantially higher number of piroplasmid parasites than vertebrate host species exist. Accordingly, the infection of a vertebrate host species by multiple piroplasmid species from the same and/or different phylogenetic lineages is commonly observed. Molecular phylogeny using 18S rRNA genes of piroplasmids infecting domestic mammals results in the formation of six clades, which emerge due to an anthropocentric research scope, but not due to a possibly assumed biological priority position. Scrutinizing the topology of inferred trees reveals stunning insights into some evolutionary patterns exhibited by this intriguing group of parasites. Contrary to expectations, diversification of parasite species appears to be dominated by host-parasite cospeciation (Fahrenholz’s rule), and, except for piroplasmids that segregate into Clade VI, host switching is rarely observed. When only domestic mammalian hosts are taken into account, Babesia sensu lato (s.l.) parasites of Clades I and II infect only dogs and cats, respectively, Cytauxzoon spp. placed into Clade III only infect cats, Theileria placed into Clade IV exclusively infect horses, wheras Theileria sensu stricto (s.s.) of Clade V infects only cattle and small ruminants. In contrast, Babesia s.s. parasites of Clade VI infect all farm and companion animal species. We outline how the unique ability of transovarial transmission of Babesia s.s. piroplasmids of Clade VI facilitates species diversification by host switching to other host vertebrate species. Finally, a deterioration of sequence fidelity in databases is observed which will likely lead to an increased risk of artifactual research in this area. Possible measures to reverse and/or avoid this threat are discussed.Instituto de PatobiologíaFil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ganzinelli Sabrina Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Ganzinelli Sabrina Belen. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Bhoora, Raksha. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases; SudáfricaFil: Omondi, David. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; AlemaniaFil: Omondi, David. Egerton University Njoro Campus. Department of Biochemistry and Molecular Biology; KeniaFil: Nijhof, Ard M. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; AlemaniaFil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaSpringer2022-08-05T10:15:27Z2022-08-05T10:15:27Z2022-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/12500https://link.springer.com/article/10.1007/s00436-022-07424-81432-1955https://doi.org/10.1007/s00436-022-07424-8Parasitology Research 121 (5) : 1207-1245 (May 2022)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repograntAgreement/INTA/2019-PE-E5-I109-001/2019-PE-E5-I109-001/AR./Convocatoria: Estudios para el control de enfermedades subtropicales y/o transmitidas por vectores (Tristeza Bovina, Garrapatas, Miasis, Tripanosomiasis, Lengua Azul y lainfo:eu-repo/semantics/restrictedAccess2025-09-04T09:49:30Zoai:localhost:20.500.12123/12500instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-04 09:49:31.065INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
title The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
spellingShingle The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
Schnittger, Leonhard
Phylogeny
Piroplasmea
Cattle
Sheep
Dogs
Cats
Goats
Horses
Evolution
Filogenia
Piroplásmea
Ganado Bovino
Ovinos
Perro
Gato
Caprinos
Caballos
Babesia
Cytauxzoon
Theileria
Evolución
title_short The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
title_full The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
title_fullStr The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
title_full_unstemmed The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
title_sort The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals : species compilation, molecular phylogeny, and evolutionary insights
dc.creator.none.fl_str_mv Schnittger, Leonhard
Ganzinelli, Sabrina Belen
Bhoora, Raksha
Omondi, David
Nijhof, Ard M.
Florin-Christensen, Mónica
author Schnittger, Leonhard
author_facet Schnittger, Leonhard
Ganzinelli, Sabrina Belen
Bhoora, Raksha
Omondi, David
Nijhof, Ard M.
Florin-Christensen, Mónica
author_role author
author2 Ganzinelli, Sabrina Belen
Bhoora, Raksha
Omondi, David
Nijhof, Ard M.
Florin-Christensen, Mónica
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv Phylogeny
Piroplasmea
Cattle
Sheep
Dogs
Cats
Goats
Horses
Evolution
Filogenia
Piroplásmea
Ganado Bovino
Ovinos
Perro
Gato
Caprinos
Caballos
Babesia
Cytauxzoon
Theileria
Evolución
topic Phylogeny
Piroplasmea
Cattle
Sheep
Dogs
Cats
Goats
Horses
Evolution
Filogenia
Piroplásmea
Ganado Bovino
Ovinos
Perro
Gato
Caprinos
Caballos
Babesia
Cytauxzoon
Theileria
Evolución
dc.description.none.fl_txt_mv The order Piroplasmida, including the genera Babesia, Cytauxzoon, and Theileria is often referred to as piroplasmids and comprises of dixenous hemoprotozoans transmitted by ticks to a mammalian or avian host. Although piroplasmid infections are usually asymptomatic in wild animals, in domestic animals, they cause serious or life-threatening consequences resulting in fatalities. Piroplasmids are particularly notorious for the enormous economic loss they cause worldwide in livestock production, the restrictions they pose on horse trade, and the negative health impact they have on dogs and cats. Furthermore, an increasing number of reported human babesiosis cases are of growing concern. Considerable international research and epidemiological studies are done to identify existing parasite species, reveal their phylogenetic relationships, and develop improved or new drugs and vaccines to mitigate their impact. In this review, we present a compilation of all piroplasmid species, isolates, and species complexes that infect domestic mammals and which have been well defined by molecular phylogenetic markers. Altogether, 57 taxonomic piroplasmid entities were compiled, comprising of 43 piroplasmid species, 12 well-defined isolates awaiting formal species description, and two species complexes that possibly mask additional species. The extrapolation of the finding of at least 57 piroplasmid species in only six domestic mammalian groups (cattle, sheep, goat, horse, dog, and cat) allows us to predict that a substantially higher number of piroplasmid parasites than vertebrate host species exist. Accordingly, the infection of a vertebrate host species by multiple piroplasmid species from the same and/or different phylogenetic lineages is commonly observed. Molecular phylogeny using 18S rRNA genes of piroplasmids infecting domestic mammals results in the formation of six clades, which emerge due to an anthropocentric research scope, but not due to a possibly assumed biological priority position. Scrutinizing the topology of inferred trees reveals stunning insights into some evolutionary patterns exhibited by this intriguing group of parasites. Contrary to expectations, diversification of parasite species appears to be dominated by host-parasite cospeciation (Fahrenholz’s rule), and, except for piroplasmids that segregate into Clade VI, host switching is rarely observed. When only domestic mammalian hosts are taken into account, Babesia sensu lato (s.l.) parasites of Clades I and II infect only dogs and cats, respectively, Cytauxzoon spp. placed into Clade III only infect cats, Theileria placed into Clade IV exclusively infect horses, wheras Theileria sensu stricto (s.s.) of Clade V infects only cattle and small ruminants. In contrast, Babesia s.s. parasites of Clade VI infect all farm and companion animal species. We outline how the unique ability of transovarial transmission of Babesia s.s. piroplasmids of Clade VI facilitates species diversification by host switching to other host vertebrate species. Finally, a deterioration of sequence fidelity in databases is observed which will likely lead to an increased risk of artifactual research in this area. Possible measures to reverse and/or avoid this threat are discussed.
Instituto de Patobiología
Fil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ganzinelli Sabrina Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Ganzinelli Sabrina Belen. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Bhoora, Raksha. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases; Sudáfrica
Fil: Omondi, David. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; Alemania
Fil: Omondi, David. Egerton University Njoro Campus. Department of Biochemistry and Molecular Biology; Kenia
Fil: Nijhof, Ard M. Freie Universität Berlin. Institute for Parasitology and Tropical Veterinary Medicine; Alemania
Fil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description The order Piroplasmida, including the genera Babesia, Cytauxzoon, and Theileria is often referred to as piroplasmids and comprises of dixenous hemoprotozoans transmitted by ticks to a mammalian or avian host. Although piroplasmid infections are usually asymptomatic in wild animals, in domestic animals, they cause serious or life-threatening consequences resulting in fatalities. Piroplasmids are particularly notorious for the enormous economic loss they cause worldwide in livestock production, the restrictions they pose on horse trade, and the negative health impact they have on dogs and cats. Furthermore, an increasing number of reported human babesiosis cases are of growing concern. Considerable international research and epidemiological studies are done to identify existing parasite species, reveal their phylogenetic relationships, and develop improved or new drugs and vaccines to mitigate their impact. In this review, we present a compilation of all piroplasmid species, isolates, and species complexes that infect domestic mammals and which have been well defined by molecular phylogenetic markers. Altogether, 57 taxonomic piroplasmid entities were compiled, comprising of 43 piroplasmid species, 12 well-defined isolates awaiting formal species description, and two species complexes that possibly mask additional species. The extrapolation of the finding of at least 57 piroplasmid species in only six domestic mammalian groups (cattle, sheep, goat, horse, dog, and cat) allows us to predict that a substantially higher number of piroplasmid parasites than vertebrate host species exist. Accordingly, the infection of a vertebrate host species by multiple piroplasmid species from the same and/or different phylogenetic lineages is commonly observed. Molecular phylogeny using 18S rRNA genes of piroplasmids infecting domestic mammals results in the formation of six clades, which emerge due to an anthropocentric research scope, but not due to a possibly assumed biological priority position. Scrutinizing the topology of inferred trees reveals stunning insights into some evolutionary patterns exhibited by this intriguing group of parasites. Contrary to expectations, diversification of parasite species appears to be dominated by host-parasite cospeciation (Fahrenholz’s rule), and, except for piroplasmids that segregate into Clade VI, host switching is rarely observed. When only domestic mammalian hosts are taken into account, Babesia sensu lato (s.l.) parasites of Clades I and II infect only dogs and cats, respectively, Cytauxzoon spp. placed into Clade III only infect cats, Theileria placed into Clade IV exclusively infect horses, wheras Theileria sensu stricto (s.s.) of Clade V infects only cattle and small ruminants. In contrast, Babesia s.s. parasites of Clade VI infect all farm and companion animal species. We outline how the unique ability of transovarial transmission of Babesia s.s. piroplasmids of Clade VI facilitates species diversification by host switching to other host vertebrate species. Finally, a deterioration of sequence fidelity in databases is observed which will likely lead to an increased risk of artifactual research in this area. Possible measures to reverse and/or avoid this threat are discussed.
publishDate 2022
dc.date.none.fl_str_mv 2022-08-05T10:15:27Z
2022-08-05T10:15:27Z
2022-05
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/12500
https://link.springer.com/article/10.1007/s00436-022-07424-8
1432-1955
https://doi.org/10.1007/s00436-022-07424-8
url http://hdl.handle.net/20.500.12123/12500
https://link.springer.com/article/10.1007/s00436-022-07424-8
https://doi.org/10.1007/s00436-022-07424-8
identifier_str_mv 1432-1955
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repograntAgreement/INTA/2019-PE-E5-I109-001/2019-PE-E5-I109-001/AR./Convocatoria: Estudios para el control de enfermedades subtropicales y/o transmitidas por vectores (Tristeza Bovina, Garrapatas, Miasis, Tripanosomiasis, Lengua Azul y la
dc.rights.none.fl_str_mv info:eu-repo/semantics/restrictedAccess
eu_rights_str_mv restrictedAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
dc.source.none.fl_str_mv Parasitology Research 121 (5) : 1207-1245 (May 2022)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
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instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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