Population genetics of Toxoplasma gondii: New perspectives from parasite genotypes in wildlife

doi:10.1016/j.vetpar.2011.07.018

Veterinary Parasitology

Volume 182, Issue 1, 24 November 2011, Pages 96-111

https://doi.org/10.1016/j.vetpar.2011.07.018 Get rights and content

Abstract

Toxoplasma gondii, a zoonotic protozoal parasite, is well-known for its global distribution and its ability to infect virtually all warm-blooded vertebrates. Nonetheless, attempts to describe the population structure of T. gondii have been primarily limited to samples isolated from humans and domesticated animals. More recent studies, however, have made efforts to characterize T. gondii isolates from a wider range of host species and geographic locales. These findings have dramatically changed our perception of the extent of genetic diversity in T. gondii and the relative roles of sexual recombination and clonal propagation in the parasite's lifecycle. In particular, identification of novel, disease-causing T. gondii strains in wildlife has raised concerns from both a conservation and public health perspective as to whether distinct domestic and sylvatic parasite gene pools exist. If so, overlap of these cycles may represent regions of high probability of disease emergence. Here, we attempt to answer these key questions by reviewing recent studies of T. gondii infections in wildlife, highlighting those which have advanced our understanding of the genetic diversity and population biology of this important zoonotic pathogen.

Section snippets

Lifecycle

Toxoplasma gondii is an apicomplexan parasite and the most extensively studied of the tissue encysting coccidia, a group that comprises many species of human and veterinary medical importance, including members of the genera Sarcocystis, Neospora, Hammondia and Besnoitia. The T. gondii lifecycle involves an asexual stage in intermediate hosts and a sexual stage in a definitive host, which may be any species of domestic or wild cat (Dubey and Frenkel, 1972, Hutchison, 1965). Cats are naturally

History

Several techniques for detecting and characterizing T. gondii genetic material either directly from infected host tissues or from parasites isolated via bioassay in mice, cats, or tissue culture have been developed. Here, we will discuss a subset of these techniques and their relative advantages and disadvantages as pertinent to the subject matter at hand. We refer the reader to a recent extensive review of molecular genotyping of T. gondii for further details (Su et al., 2010). To adequately

Sylvatic and domestic cycles: do they exist?

The high diversity in T. gondii genotypes isolated from wildlife samples as compared to those from domestic animals raises the question as to whether distinct gene pools exist for domestic and sylvatic hosts. The relevance of this question derives from concern that when distinct parasite gene pools overlap, most likely due to human environmental encroachment, disease outbreaks may occur in either human/domestic animal or wildlife populations due to exposure of hosts to novel parasite genotypes (

Conclusions and future directions

The most important conclusion that can be drawn from recent genotyping efforts of T. gondii isolates from wildlife is that the so-called ‘exotic’ or ‘atypical’ strains are not insignificant anomalies in the population structure of this parasite, but rather important members of the gene pool that provide a much better representation of the vast host range utilized by this parasite. There are clearly genotypes that dominate in the T. gondii population in addition to the originally identified

Conflict of interest

The authors declare that there is no conflict of interest.

Acknowledgements

Thanks to all members of the Grigg lab for helpful discussions. This work was supported by the Intramural Research program of the NIH and NIAID, grant # AI001018 and The Morris Animal Foundation wildlife training fellowship grant # D10ZO-416 (JMW). MEG is a scholar of the Canadian Institute for Advanced Research (CIFAR) Program for Integrated Microbial Biodiversity.

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Citation Excerpt :
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Routine post mortems of deceased penguins from Penguin Island, Western Australia, found that a temporal cluster of cases presented with characteristic gross and microscopic changes, namely birds in good body condition with hepatomegaly and splenomegaly, multifocal hepatic and splenic necrosis and numerous, 1–2 μm diameter protozoan parasites within the necrotic foci.
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Population genetics of Toxoplasma gondii: New perspectives from parasite genotypes in wildlife

Abstract

Section snippets

Lifecycle

History

Sylvatic and domestic cycles: do they exist?

Conclusions and future directions

Conflict of interest

Acknowledgements

Int. J. Parasitol.

Int. J. Parasitol.

Vet. Parasitol.

Int. J. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Curr. Opin. Microbiol.

Int. J. Parasitol.

Int. J. Parasitol.

J. Infect.

Int. J. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Int. J. Parasitol.

Vet. Parasitol.

Int. J. Parasitol.

Vet. Parasitol.

Vet. Parasitol.

Int. J. Parasitol.

Parasitol. Today

Int. J. Parasitol.

Genotype of 86 Toxoplasma gondii isolates associated with human congenital toxoplasmosis, and correlation with clinical findings

J. Infect. Dis.

Genetic diversity of Toxoplasma gondii isolates in egyptian feral cats reveals new genotypes

J. Parasitol.

The evolutionary genomics of pathogen recombination

Nat. Rev. Genet.

Toxoplasmosis in a woodchuck (Marmota monax) and two American red squirrels (Tamiasciurus hudsonicus)

J. Vet. Diagn. Invest.

The role of wildlife in emerging and re-emerging zoonoses

Rev. Sci. Tech.

High-resolution typing of Toxoplasma gondii using microsatellite loci

J. Parasitol.

Direct genotypic characterization of Toxoplasma gondii strains associated with congenital toxoplasmosis in Tunisia (North Africa)

Am. J. Trop. Med. Hyg.

Toxoplasmosis in Indo-Pacific humpbacked dolphins (Sousa chinensis), from Queensland

Aust. Vet. J.

Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii

Proc. Natl. Acad. Sci. U.S.A.

Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence

Philos. Trans. R. Soc. Lond. B Biol. Sci.

Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis)

J. Parasitol.

Sex determination and sex differentiation in coccidia: gametogony and oocyst production after monoclonal infection of cats with free-living and intermediate host stages of Isospora (Toxoplasma) gondii

Parasitology

Genotypic characterization of Toxoplasma gondii in sheep from Brazilian slaughterhouses: new atypical genotypes and the clonal type II strain identified

Vet. Parasitol.

Cats and Toxoplasma: implications for public health

Zoonoses Public Health

Isoenzymic characterization of seven strains of Toxoplasma gondii by isoelectrofocusing in polyacrylamide gels

Am. J. Trop. Med. Hyg.

Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiological implications

J. Parasitol.

Emerging infectious diseases of wildlife—threats to biodiversity and human health

Science

Fatal outbreak of human toxoplasmosis along the Maroni River: epidemiological, clinical, and parasitological aspects

Clin. Infect. Dis.

Toxoplasmosis in mynahs

Avian Dis.

Cerebral toxoplasmosis in striped dolphins (Stenella coeruleoalba) stranded along the Ligurian Sea coast of Italy

Vet. Pathol.

Infectivity and pathogenicity of Toxoplasma gondii oocysts for cats

J. Parasitol.

Pathogenicity and infectivity of Toxoplasma gondii oocysts for rats

J. Parasitol.

Tissue cyst tropism in Toxoplasma gondii: a comparison of tissue cyst formation in organs of cats, and rodents fed oocysts