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Comparative Study
. 2011 Jun;5(6):e1155.
doi: 10.1371/journal.pntd.0001155. Epub 2011 Jun 7.

Comparative microsatellite typing of new world leishmania infantum reveals low heterogeneity among populations and its recent old world origin

Affiliations
Comparative Study

Comparative microsatellite typing of new world leishmania infantum reveals low heterogeneity among populations and its recent old world origin

Katrin Kuhls et al. PLoS Negl Trop Dis. 2011 Jun.

Abstract

Leishmania infantum (syn. L. chagasi) is the causative agent of visceral leishmaniasis (VL) in the New World (NW) with endemic regions extending from southern USA to northern Argentina. The two hypotheses about the origin of VL in the NW suggest (1) recent importation of L. infantum from the Old World (OW), or (2) an indigenous origin and a distinct taxonomic rank for the NW parasite. Multilocus microsatellite typing was applied in a survey of 98 L. infantum isolates from different NW foci. The microsatellite profiles obtained were compared to those of 308 L. infantum and 20 L. donovani strains from OW countries previously assigned to well-defined populations. Two main populations were identified for both NW and OW L. infantum. Most of the NW strains belonged to population 1, which corresponded to the OW MON-1 population. However, the NW population was much more homogeneous. A second, more heterogeneous, population comprised most Caribbean strains and corresponded to the OW non-MON-1 population. All Brazilian L. infantum strains belonged to population 1, although they represented 61% of the sample and originated from 9 states. Population analysis including the OW L. infantum populations indicated that the NW strains were more similar to MON-1 and non-MON-1 sub-populations of L. infantum from southwest Europe, than to any other OW sub-population. Moreover, similarity between NW and Southwest European L. infantum was higher than between OW L. infantum from distinct parts of the Mediterranean region, Middle East and Central Asia. No correlation was found between NW L. infantum genotypes and clinical picture or host background. This study represents the first continent-wide analysis of NW L. infantum population structure. It confirmed that the agent of VL in the NW is L. infantum and that the parasite has been recently imported multiple times to the NW from southwest Europe.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Distribution of the populations and subpopulations of NW L. infantum in the studied endemic regions.
The first number refers to the number of strains belonging to the indicated population (specified by the color), the second number gives the overall number of studied strains from the respective region. Additional endemic regions that were not studied are marked by grey color. (A): Colors of the respective population correlate with those in Fig. 2 (Pop1-INFNW - blue; Pop2-INFNW - red). In Honduras all but one strain belong to Population 1. In Colombia shared memberships in both populations could be recognized, with the predominant part of membership in Population 1. (B): Sub-populations found in Population 1. Colors correlate with those of the sub-populations in Fig. 2 (Sub-Pop1A-INFNW - dark blue, Sub-Pop1B-INFNW - light blue). In Pará one strain belongs to Sub-Pop1A-INFNW, and two strains have shared membership in both sub-populations 1A and 1B with predominating 1B traits, and two strains belong to sub-population 1B. Strains from Colombia belong to the 1B subpopulation (light blue), the Hondurian strains to 1A (dark blue) (not shown). (C): Distribution of clinical pictures among the 98 studied strains. VL – visceral leishmaniasis, CL – cutaneous leishmaniasis, CanL – canine leishmaniasis, nd – not determined.
Figure 2
Figure 2. Estimated population structure and substructure of NW L. infantum as inferred by the STRUCTURE program.
Results are based on MLMT of 14 microsatellite markers obtained for the 98 strains of NW L. infantum studied. In the barplots each strain is represented by a single vertical line divided into K colors, where K is the number of populations assumed. Each color represents one population, and the length of the colors segment shows the strain's estimated proportion of membership in that population. Isolates are organized by membership coefficients. According to ΔK the most probable number of populations in the data set is two, corresponding to MON-1 (blue) and non-MON-1 (red) isolates. In each of these main populations ΔK calculations suggest two sub-populations. VL – visceral leishmaniasis, CL – cutaneous leishmaniasis, CanL – canine leishmaniasis.
Figure 3
Figure 3. Neighbor-joining tree inferred from the Chord-distance calculated for the MLMT profiles of NW L. infantum.
This unrooted tree was derived based on the MLMT profiles of 14 microsatellite markers for the studied sample set of 98 strains of NW L. infantum as used for Bayesian model-based analysis with the STRUCTURE program. The two populations inferred by STRUCTURE (K2) are found also by this distance –based method and are indicated on the tree. Strain origins are explained in the window beside. Marsupial and fox isolates are marked by triangles. VL – visceral leishmaniasis, CL – cutaneous leishmaniasis, CanL – canine leishmaniasis.
Figure 4
Figure 4. Estimated population structure and substructure of the combined New World and Old World sample set.
MLMT profiles based on 14 microsatellite markers for 308 OW strains and 98 NW strains of L. infantum were analysed by Bayesian statistics implemented in the STRUCTURE software. In the barplots each strain is represented by a single vertical line divided into K colors, where K is the number of populations assumed. Each color represents one population, and the length of the colors segment shows the strain's estimated proportion of membership in that population. Isolates are organized by membership coefficients. According to ΔK the most probable number of populations in the data set is three, corresponding to MON-1 isolates from Southwest Europe and the New World (blue), MON-1 isolates from North Africa, Southeast Europe and Asia (green), and non-MON-1 islates from the Old and New World (red). ΔK calculations suggest two sub-populations in the main populations Pop1 and Pop3.
Figure 5
Figure 5. Neighbor-joining tree derived for the combined New World and Old World data set.
This unrooted tree was inferred from the Chord-distance calculated for the MLMT profiles of 14 microsatellite markers for the studied sample set of 98 NW strains of L. infantum (marked by blue squares), 308 OW strains of L. infantum (marked by dots of different colors, depending on their origin) and 20 strains of L. donovani (marked by grey triangles). The three populations inferred by Bayesian model-based analysis with the STRUCTURE program (K3) and shown in Fig. 4 are indicated. MON-1 strains are marked by blue branches, non-MON-2 strains by red branches, and L. donovani by black branches. NW strains of L. infantum are present in population 1 and 3. Strains isolated from Didelphis marsupialis and Cerdocyon thous are interspersed among population1 that included the majority of NW strains (human and canine) together with strains of L. infantum from the Iberian mainland (Spain, Portugal), France and Italy. Strain origins are listed in the legend beside.
Figure 6
Figure 6. Map showing the presumable origin of NW L. infantum.
The respective populations of L. infantum in the Old and New Worlds are indicated by the respective colors used in Fig. 2 and 5. NW L. infantum has been introduced from Southwest Europe to the New World multiple times.

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