The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: species compilation, molecular phylogeny, and evolutionary insights.
Abstract: 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.
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This article focuses on Piroplasmida parasites, including the Babesia, Cytauxzoon, and Theileria genera, that are transmitted by ticks to their hosts, and often cause serious consequences in domestic animals. The research presents a compilation of these species and offers detailed insights into their molecular phylogeny and evolution.
Piroplasmida parasites and their impact
The study focuses on piroplasmid parasites known to be transmitted to hosts by ticks. These hosts can include an array of animals, from farm and companion animals to birds.
While these infections are usually asymptomatic in wild animals, for domestic animals, they can lead to serious health complications and even death.
These parasites have significant global economic impact, causing a decrease in livestock productivity, restrictions on horse trade, and health issues in domestic pets.
The rise in reported human cases of babesiosis, a disease caused by these parasites, is an increasing concern.
Compilation of Piroplasmida species and Phylogeny
The review provides a detailed overview of all identified piroplasmid species that affect domestic mammals.
They have identified 57 taxonomic entities of these parasites, which are comprised of 43 species, 12 isolates awaiting formal species descriptions, and two species complexes that possibly mask additional species.
The molecular phylogeny of these parasites reveals six distinct clades or branches, giving interesting insights into their evolutionary patterns.
Evolutionary insights and host-parasite relationships
The study highlighted that contrary to expectations, the evolution of parasite species seems dominated by coevolution with their hosts (Fahrenholz’s rule).
The ability of these parasites to infect multiple host species is noted, particularly in the case of Babesia s.s. parasites from Clade VI, which can infect all farm and companion animal species.
The research also discussed the potential of host switching and how that contributes to the diversification of species, specifically noting how transovarial transmission (from parent to offspring) in Babesia s.s. piroplasmids of Clade VI aids species diversification.
Issues with database fidelity
This research highlights an observed issue in sequence fidelity in databases, which can potentially increase the risk of inaccurate research in this field.
The article concludes with a discussion on possible measures that could be used to prevent or reverse this problem.
Cite This Article
APA
Schnittger L, Ganzinelli S, Bhoora R, Omondi D, Nijhof AM, Florin-Christensen M.
(2022).
The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: species compilation, molecular phylogeny, and evolutionary insights.
Parasitol Res, 121(5), 1207-1245.
https://doi.org/10.1007/s00436-022-07424-8
Instituto de Patobiología Veterinaria (IPVET), CICVyA, INTA-Castelar, Los Reseros y Nicolas Repetto, s/n, 1686, Hurlingham, Buenos Aires, Argentina. schnittger.leonhard@inta.gob.ar.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina. schnittger.leonhard@inta.gob.ar.
Ganzinelli, Sabrina
Instituto de Patobiología Veterinaria (IPVET), CICVyA, INTA-Castelar, Los Reseros y Nicolas Repetto, s/n, 1686, Hurlingham, Buenos Aires, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
Bhoora, Raksha
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa.
Omondi, David
Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, 14163, Berlin, Germany.
Department of Biochemistry and Molecular Biology, Egerton University Njoro Campus, P.O. Box 536, Egerton, 20115, Kenya.
Nijhof, Ard M
Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, 14163, Berlin, Germany.
Florin-Christensen, Mónica
Instituto de Patobiología Veterinaria (IPVET), CICVyA, INTA-Castelar, Los Reseros y Nicolas Repetto, s/n, 1686, Hurlingham, Buenos Aires, Argentina.
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina.
MeSH Terms
Animals
Babesia
Babesiosis / parasitology
Cat Diseases
Cats
Cattle
Dog Diseases / parasitology
Dogs
Farms
Haemosporida / genetics
Horses
Mammals
Phylogeny
Piroplasmida
RNA, Ribosomal, 18S / genetics
Sheep / genetics
Theileria / genetics
Grant Funding
2019-PD-E5-I109-001 / Instituto Nacional de Tecnologu00eda Agropecuaria
2019-PD-E5-I103-001 / Instituto Nacional de Tecnologu00eda Agropecuaria
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