Combining spatial analysis and host population genetics to gain insights into the mode of transmission of a pathogen: The example of Toxoplasma gondii in mice.

Toxoplasma gondii is a ubiquitous highly prevalent zoonotic protozoan. Cats are the definitive hosts, while all other warm-blooded animals are intermediate hosts for this parasite. Commensal rodents, being the main prey of cats, are probably the major reservoir for T. gondii in the domestic environment. Rodents can acquire infection after ingestion of oocysts that have sporulated in the environment. However, experimental evidence shows that vertical transmission can be sufficient for the perpetuation of transmission between generations of mice. In natural settings, the relative epidemiological importance of vertical transmission over oral transmission is a matter of debate and raises the question of the possibility of a T. gondii cycle in the absence of cats. In the present study, we took advantage of an extensive survey of commensal rodents in Dakar, Senegal, where the house mouse is the predominant putative reservoir of T. gondii. Mice genotypes and spatial location through GPS referencing of all trapping localizations were investigated in relation to T. gondii infection in eight sites of the city of Dakar and on Goree Island. In each sampling site, the occurrence of over-prevalence zones of T. gondii infection was investigated through Kulldorf's statistic using SaTScan software. Genetic structure and relatedness between mice were investigated within each over-prevalence zone, in order to find clues of transmission between related mice. Within each of the four over-prevalence zones identified across nine sites, infected mice belonged to more than one genetic group. No association between the degree of relatedness and the occurrence of T. gondii infection could be detected. These findings suggest an environmental source of infection for mice associated with localized putative foci of environmental contamination and support an oral route of infection for mice from Dakar rather than a cycle based on vertical transmission. However, further investigations based on a denser sampling in different epidemiological contexts are recommended.

Diversity of Toxoplasma gondii strains shaped by commensal communities of small mammals.

Commensal rodent species are key reservoirs for Toxoplasma gondii in the domestic environment. In rodents, different T. gondii strains show variable patterns of virulence according to host species. Toxoplasma gondii strains causing non-lethal chronic infections in local hosts will be more likely to persist in a given environment, but few studies have addressed the possible role of these interactions in shaping the T. gondii population structure. In addition, the absence of validated techniques for upstream detection of T. gondii chronic infection in wild rodents hinders exploration of this issue under natural conditions. In this study, we took advantage of an extensive survey of commensal small mammals in three coastal localities of Senegal, with a species assemblage constituted of both native African species and invasive species. We tested 828 individuals for T. gondii chronic infection using the modified agglutination test for antibody detection in serum samples and a quantitative PCR assay for detection of T. gondii DNA in brain samples. The infecting T. gondii strains were genotyped whenever possible by the analysis of 15 microsatellite markers. We found (i) a very poor concordance between molecular detection and serology in the invasive house mouse, (ii) significantly different levels of prevalence by species and (iii) the autochthonous T. gondii Africa 1 lineage strains, which are lethal for laboratory mice, only in the native African species of commensal small mammals. Overall, this study highlights the need to reconsider the use of MAT serology in natural populations of house mice and provides the first known data about T. gondii genetic diversity in invasive and native species of small mammals from Africa. In light of these results, we discuss the role of invasive and native species, with their variable adaptations to different T. gondii strains, in shaping the spatial structure of T. gondii genetic diversity in Africa.