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. 2011 Oct;5(10):e1363.
doi: 10.1371/journal.pntd.0001363. Epub 2011 Oct 11.

Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids

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Recent, independent and anthropogenic origins of Trypanosoma cruzi hybrids

Michael D Lewis et al. PLoS Negl Trop Dis. 2011 Oct.

Abstract

The single celled eukaryote Trypanosoma cruzi, a parasite transmitted by numerous species of triatomine bug in the Americas, causes Chagas disease in humans. T. cruzi generally reproduces asexually and appears to have a clonal population structure. However, two of the six major circulating genetic lineages, TcV and TcVI, are TcII-TcIII inter-lineage hybrids that are frequently isolated from humans in regions where chronic Chagas disease is particularly severe. Nevertheless, a prevalent view is that hybridisation events in T. cruzi were evolutionarily ancient and that active recombination is of little epidemiological importance. We analysed genotypes of hybrid and non-hybrid T. cruzi strains for markers representing three distinct evolutionary rates: nuclear GPI sequences (n = 88), mitochondrial COII-ND1 sequences (n = 107) and 28 polymorphic microsatellite loci (n = 35). Using Maximum Likelihood and Bayesian phylogenetic approaches we dated key evolutionary events in the T. cruzi clade including the emergence of hybrid lineages TcV and TcVI, which we estimated to have occurred within the last 60,000 years. We also found evidence for recent genetic exchange between TcIII and TcIV and between TcI and TcIV. These findings show that evolution of novel recombinants remains a potential epidemiological risk. The clearly distinguishable microsatellite genotypes of TcV and TcVI were highly heterozygous and displayed minimal intra-lineage diversity indicative of even earlier origins than sequence-based estimates. Natural hybrid genotypes resembled typical meiotic F1 progeny, however, evidence for mitochondrial introgression, absence of haploid forms and previous experimental crosses indicate that sexual reproduction in T. cruzi may involve alternatives to canonical meiosis. Overall, the data support two independent hybridisation events between TcII and TcIII and a recent, rapid spread of the hybrid progeny in domestic transmission cycles concomitant with, or as a result of, disruption of natural transmission cycles by human activities.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Maximum likelihood tree of GPI sequences (unique haplotypes).
Four major clades are indicated according to corresponding T. cruzi lineage; TcV and TcVI haplotypes are within the parental TcII and TcIII clades from which they are derived. Where clear geographic associations were evident these are indicated: US (samples from USA); SA (samples from South America); ‘Northern’ and ‘Southern’ groups within TcIII are as defined previously . Branches separating T. cruzi from T. rangeli and T. brucei (outgroup) are not shown. Bootstrap support values for branches (if >50%) are shown and were calculated for the equivalent nodes of the bootstrap consensus NJ/MP trees (1000 replicates). Scale units are substitutions/site.
Figure 2
Figure 2. Maximum likelihood tree of COII-ND1 sequences (unique haplotypes).
Clades and subclades are indicated according to corresponding major T. cruzi lineage (see text). Black circles indicate TcIII haplotypes and black triangles indicate TcIV haplotypes, clearly showing paraphyly of TcIV and TcIII sequences and sharing of identical haplotypes between subsets of TcIII and TcIV samples. Where clear geographic associations were evident these are indicated using standard two letter country codes; TcIV(SA) are TcIV samples from South America. Bootstrap support values for branches (if >50%) are shown and were calculated for the equivalent nodes of the bootstrap consensus NJ/MP trees (1000 replicates). Scale units are substitutions/site.
Figure 3
Figure 3. Unrooted neighbour-joining microsatellite D AS trees showing lack of diversity within hybrid lineages TcV and TcVI.
A) Tree based on 28 loci typed across 35 samples from parental (TcII, TcIII) and hybrid (TcV, TcVI) lineages. B) Tree based on 19 loci typed across 81 samples from all six major lineages TcI-VI. D AS-based bootstrap values were calculated over 1000 trees from pseudo-replicate datasets and those >70% are shown for the relevant nodes.
Figure 4
Figure 4. Patterns of microsatellite allelic inheritance in hybrid lineages TcV and TcVI.
Based on analysis of 19 locus and 28 locus data sets combined. A) For each parental (TcII, TcIII) and hybrid (TcV, TcVI) group the charts show the proportion of microsatellite alleles that were also found in each of the other three groups and the proportion of private alleles – those not found in any of the other three groups. B) Mean pairwise genetic identities (1-D AS) between hybrid group (TcV and TcVI) MLGs and parental group (TcII and TcIII) MLGs from different geographical regions; DTU, discrete typing unit; error bars are S.E.M; brackets represent statistically significant 2-tailed t-tests with asterisks indicating: ** p<0.01, *** p<0.001.

References

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