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A total of 6, determinations were compiled.
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These undistinguished DTUs accounted for 1. The geographical origin was informed by the country name no missing data , the upper continental subdivision of North, Central, and South America, the upper administrative divisions such as state, province, department or region, and the lower administrative divisions such as municipality, province, or community according to the information existing in the publications. The collection dates of the strain or biological samples were not always documented Host origin was generally informed by the species 31 missing data , and columns were added indicating the order, genus and tribe for the triatomines.
When the location of the capture site was missing, the wild mammals where classified in the sylvatic cycle except for the synanthropic species such as opossums and rodents for which the information was considered as unknown uk. The information on the methods used for the characterization of the DTUs is also included in S1 Table.
The first column indicates if the DTU was characterized at nuclear or mitochondrial level or both, the second one indicates the method s used, and the third one on the markers, the names of the genes, or the number of loci for MLMT multilocus microsatellite typing and MLEE multilocus enzyme electrophoresis. The 6, samples of T. The vast majority of data relate to South America The DTUs were identified in 86 genera 32 missing cases , different species of which 42 are vectors belonging to 7 genera Dipetalogaster , Eratyrus , Meccus , Mepraia , Panstrongylus , Rhodnius , and Triatoma.
Approximately of the identifications in South America The mammal species belong to nine orders of which the most represented is the Primate order One-third of the DTU identifications In the other records, TcI was found in approximatively Fig 1 presents the proportions of DTUs observed, excluding from the calculation the ambiguous DTU determinations over the entire endemic area, and in North, Central and South America see below.
The ambiguous determinations of DTUs were deleted from the samples. Therefore this DTU is probably underestimated because it is not recognized by the markers used in many publications, and consequently it may have been erroneously equated with TcI. This DTU was identified in 59 bats belonging to 12 different species in Brazil, Colombia, and Ecuador [ 16 , 17 , 26 , 27 ], in one specimen of T. It was identified in all the countries included in the study. TcII was much more rarely identified 9.
It was not identified in Central America out of identifications, and only 13 identifications were reported from North America out of 2. The five other identifications were from mice and rats captured in the immediate surroundings of the dwelling of the first described autochthonous case of T. These DTUs showed the most differential geographical distribution. In contrast, in South America, these DTUs together have frequently been identified in several countries, Argentina In Peru they were identified in Moreover, when the two DTUs coexist, different proportions can be observed in the different countries.
The current results Fig 3 show that all DTUs, including Tcbat and taking into account the two cases described in the domestic cycle [ 18 , 28 ], participate in domestic and sylvatic cycles in some places. Nevertheless, these tests are only indicative because they correspond to a very gross approach that ignores sampling bias, which obviously exists. In this study, of 26 specimens of this species, TcI only reached These results suggest a remarkably high diversity of DTUs in this genus. Among them, TcIV was the most common 4. It was identified in three species: R. TcII was identified in only three R.
In contrast, in the genera Mepraia and Triatoma although TcI remains a major strain In Mepraia , the identifications were made in two species M. In the genus Triatoma , the data were available for 18 species Table 2 , but the results concerned principally T. Lower numbers of DTU identifications were available for T.
For the remaining species, there were fewer than ten identifications. Although T. Domestic cycles. Considering domestic cycles and their mammalian hosts, most of the identifications made were from samples isolated from humans identifications, Those in dogs reached , from nine countries.
Sixteen identifications were from cats from Argentina [ 56 , 57 ], 91 others were from small rodents in six countries that readily nest in peridomestic structures e. There was also a single study of DTU identification in 24 goats in Chile [ 58 ]. TcV was more abundant than TcVI in humans and conversely in dogs.
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For small rodents, TcI predominated. Moreover, TcV was found in R. Sylvatic cycles. In the wild environment, the identifications of T. For the orders, Artiodactyla [ 47 , 60 ] and Pilosa [ 10 , 24 , 61 , 62 ], which included no more than five identifications each, all were TcI. For the other orders, several specific trends are detailed below.
The identifications in Didelphimorphia were from 12 countries in North and South America, and from 20 species. In the order Chiroptera, identifications were reported in 23 species, all from South America.
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In the order Carnivora, TcI However, the majority of the sample was from Chile For the wild primates, a total of 51 identifications were made in 15 monkey species mostly sampled in Brazil For many years, the characterization of T. The current compilation, based on the consensus nomenclature of six DTUs, reached an accumulated number of 6, identifications. However, T. Despite of this nonexhaustive list of biases, the data reported herein constitute the most complete picture of the DTU distribution in the endemic area of Chagas disease.
The purpose of this review is not to discuss the current nomenclature of T. Indeed, there is an increasing number of new genetic analyses of T. These last few years, a number of studies aiming to characterize T. Based on the available typing data, the first outstanding result is the predominance of TcI strains. This DTU, genetically diversified, is found throughout the geographic distribution of T. There are probably no ecological systems i. However, it appears that TcI strains do not develop well in some mammal species such as those within the order Cingulata since this order is rarely infected with TcI Table 3.
TcI is an old DTU that has evolved since 3—16 MYA as previously proposed [ 71 ], and its very high genetic diversity is consistent with a long-term evolution. Moreover, recombination between TcI strains appears to be more frequent than previously thought [ 2 , 3 , 72 ]. The recombination events i. Another question is the geographical origin of TcI. A North-South clustering was recognized, even if some incongruence remains to be explained [ 73 — 75 ]. It should be noted that if the current trend is to propose sub groups within TcI, the presence of subunits, evolving separately, must be previously evidenced which is not yet the case.
Also, it has been proposed that marsupial species of the family Didelphidae family are the ancestral hosts of TcI [ 78 ] given that, among others, TcI predominates in these animals. Based on our recent analysis of COII and CytB gene sequences previously deposited in GenBank [ 8 ], we evaluated the haplotype and nucleotide diversities of TcI within the order Didelphimorphia, and we observed that these indices were comparable to those obtained for all the other orders of wild mammals combined.
This assesses the larger genetic diversity in marsupials than in other animals, supporting a longer association.
The remarkable expansion of TcI, which invaded most of environments, does not allow its origin to be determined from the picture of its geographical distribution alone. A similar level of differences is also observed for nucleotide diversity.
The available data on the geographical distribution of TcII suggest that it is absent or extremely rare in some ecosystems Central and North America. It seems that TcII strains would not have had the same expansion capacity as TcI among the wild cycles, and they probably found refuge mostly in certain wild mammals. However, its strong association with primates in the Atlantic Coastal Rainforest in Brazil should be noted [ 79 ].
For now, its geographical distribution is more consistent with a South American origin, and further south than north of the Amazon basin where this DTU is more abundant. First, it is important to note that the genetic data do not clearly define these two groups separately. Several studies showed that these strains are the result of ancient hybridization s between TcI and TcII strains, which suffer over time from genetic rearrangements, decreasing their level of heterozygosity at the expense of mosaic mitochondrial and nuclear genes [ 80 ].
Recombination events have probably occurred several times and this would have given a mtTcIII group composed of polyphyletic subgroups of strains. Therefore, the wild strains from the US, attributed to TcIV, seem to be a monophyletic subgroup differing from the others long ago [ 81 ], but whose closest ancestors have probably disappeared.
They are usually considered hybrids and they are heterozygous at several loci and SNPs single nucleotide polymorphisms. In our database, a total of Some of these strains have spread across large geographic areas through the clonal propagation mode [ 82 ]. Both DTUs are clearly associated with domestic cycles since only They are identified in some Didelphimorphia and in different species of rodents but only in the Southern Cone countries and Bolivia.
Previously, the Gran Chaco region was proposed as the original location of these DTUs, where they are very abundant and where the putative parents are also present [ 15 ], and this hypothesis fits well with the current observed distribution of these DTUs. The universe of Hemiptera vectors of T. In the current data, only 37 species of vectors are included and for the majority of them, very few DTU determinations were made, even though these vectors are generally widely distributed. Similarly, the knowledge of the parasite genetic variants that infect mammals, except for humans, and to a lesser extent for Didelphidae, is very limited.
In various regions, in a context of high anthropization and climate changes, it is urgent to study the impact of these environmental modifications on potential vectors and their hosts. Several studies of experimental infections of vectors with different strains of T. Few studies relate comparisons of DTUs in experimental infections in a single triatomine species. For T. As a field observation, we can report the case of Triatoma sordida , a primary vector in the northeast of the city of Santa Cruz, in Bolivia, in which TcI was predominantly detected while in mammals of the same area, TcV was a major strain [ 59 ].
In wild mammal hosts, experimental infections of two important reservoirs in the US placental and marsupial showed DTU-mammal association [ 87 ]. Examples could be multiplied but we can already conclude that the vectors and even the wild mammal hosts can influence the distribution of DTUs. Whatever the host, there is a balance between parasite genotypes and hosts which probably depends on environmental conditions such as outside temperature for vectors or immune and nutritional status for mammals.
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The diversity of hosts, and environmental conditions certainly explain the maintenance of parasitic diversity and the emergence of new variants by natural selection. Therefore the distribution of DTUs reported here, although very informative, is only a temporary picture that will inevitably evolve over time, above all if drastic environmental changes occur such as deforestation, intensive farming, urbanization, and unexpected climatic upheavals.
Each line corresponds to the identification of a single strain for which the geographic, host, and time origins are specified. The publication source is also presented.
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Conceived and designed the experiments: SFB. Abstract Trypanosoma cruzi , the causative agent of Chagas disease, presents wide genetic diversity. Funding: The authors received no specific funding for this work. Introduction Trypanosoma cruzi is a pathogenic microorganism, the causative agent of Chagas disease, characterized by high genetic and phenotypic intraspecific diversity.
Results General overview of available data The 6, samples of T. Download: PPT. Fig 1. Fig 2. Eco-epidemiology of the DTUs Domestic versus sylvatic cycles.