Genetic diversity and population structure of Leishmania (Viannia) braziliensis in the Peruvian jungle

Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as m...

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Published inPLoS neglected tropical diseases Vol. 16; no. 5; p. e0010374
Main Authors De los Santos, Maxy B., Ramírez, Ivonne Melissa, Rodríguez, Jorge E., Beerli, Peter, Valdivia, Hugo O.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2022
Public Library of Science (PLoS)
Subjects
Biological diversity
Biology and Life Sciences
Clusters
Colonization
Cutaneous leishmaniasis
Distribution
Earth Sciences
Ecology and Environmental Sciences
Economic activities
Equilibrium
Evaluation
Gene polymorphism
Genetic aspects
Genetic diversity
Genetic variation
Geographical distribution
Human subjects
Humans
Inbreeding
Leishmania
Leishmania braziliensis - genetics
Leishmaniasis, Cutaneous - parasitology
Linkage disequilibrium
Markers
Microsatellite Repeats
Microsatellites
Migration
Parasites
Parasitic diseases
People and places
Peru - epidemiology
Polymorphism
Polymorphism, Genetic
Population
Population biology
Population genetics
Population structure
Subpopulations
Tropical diseases
Vector-borne diseases
Vectors
Peru
Brazil
United States > US
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Abstract Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
AbstractList Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. Principal findings High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. Conclusions L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. Principal findings High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. Conclusions L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions. Author summary L. (V.) braziliensis is widespread in the Peruvian jungle region. In this region, the departments of Cusco and Madre de Dios account for a large number of patients that get infected while working in the virgin forest. For the first time, we described ample genetic diversity among Peruvian L. (V.) braziliensis isolates with new alleles that were not previously reported in South America. In addition, two different genetic clusters or subpopulations of L. (V.) braziliensis in the Amazon Rainforest of Peru were described. This finding reveals the important distribution of parasite populations and suggests a possible colonization event between ecoregions of the highland and lowland Peruvian jungle independently of recent human migration.
Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. Principal findings High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. Conclusions L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
L . (V . ) braziliensis is widespread in the Peruvian jungle region. In this region, the departments of Cusco and Madre de Dios account for a large number of patients that get infected while working in the virgin forest. For the first time, we described ample genetic diversity among Peruvian L . (V . ) braziliensis isolates with new alleles that were not previously reported in South America. In addition, two different genetic clusters or subpopulations of L . (V . ) braziliensis in the Amazon Rainforest of Peru were described. This finding reveals the important distribution of parasite populations and suggests a possible colonization event between ecoregions of the highland and lowland Peruvian jungle independently of recent human migration.
Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers. Principal findings High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive F.sub.IS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle. Conclusions L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers.BACKGROUNDHuman cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed to fight against drug trafficking and civilian people that migrate from the highland to the lowland jungle for economic activities such as mining, agriculture, construction, and chestnut harvest. We explored the genetic diversity and population structure of 124 L. (V.) braziliensis isolates collected from the highland (Junín, Cusco, and Ayacucho) and lowland Peruvian jungle (Loreto, Ucayali, and Madre de Dios). All samples were genotyped using Multilocus Microsatellite Typing (MLMT) of ten highly polymorphic markers.High polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle.PRINCIPAL FINDINGSHigh polymorphism and genetic diversity were found in Peruvian isolates of L. (V.) braziliensis. Most markers are not in Hardy-Weinberg equilibrium; this deviation is most likely caused by local inbreeding, as shown by the positive FIS values. Linkage Disequilibrium in subpopulations was not strong, suggesting the reproduction was not strictly clonal. Likewise, for the first time, two genetic clusters of this parasite were determined, distributed in both areas of the Peruvian jungle, which suggested a possible recent colonization event of the highland jungle from the lowland jungle.L. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.CONCLUSIONSL. (V.) braziliensis exhibits considerable genetic diversity with two different clusters in the Peruvian jungle. Migration analysis suggested a colonization event between geographical areas of distribution. Although no human migration was observed at the time of sampling, earlier displacement of humans, reservoirs, or vectors could have been responsible for the parasite spread in both regions.
Audience Academic
Author Beerli, Peter
Ramírez, Ivonne Melissa
De los Santos, Maxy B.
Rodríguez, Jorge E.
Valdivia, Hugo O.
AuthorAffiliation 2 Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Peru
4 Department of Scientific Computing, Florida State University, Tallahassee, Florida, United States of America
Charité University Medicine Berlin, GERMANY
1 Department of Parasitology, U.S. Naval Medical Research Unit 6, Lima, Peru
3 Unidad de Biotecnología Molecular, Universidad Peruana Cayetano Heredia, Lima, Peru
AuthorAffiliation_xml – name: 1 Department of Parasitology, U.S. Naval Medical Research Unit 6, Lima, Peru
– name: 4 Department of Scientific Computing, Florida State University, Tallahassee, Florida, United States of America
– name: Charité University Medicine Berlin, GERMANY
– name: 3 Unidad de Biotecnología Molecular, Universidad Peruana Cayetano Heredia, Lima, Peru
– name: 2 Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos, Lima, Peru
Author_xml – sequence: 1
  givenname: Maxy B.
  orcidid: 0000-0002-3379-4869
  surname: De los Santos
  fullname: De los Santos, Maxy B.
– sequence: 2
  givenname: Ivonne Melissa
  orcidid: 0000-0003-0033-6770
  surname: Ramírez
  fullname: Ramírez, Ivonne Melissa
– sequence: 3
  givenname: Jorge E.
  orcidid: 0000-0002-4193-8017
  surname: Rodríguez
  fullname: Rodríguez, Jorge E.
– sequence: 4
  givenname: Peter
  orcidid: 0000-0003-0947-5451
  surname: Beerli
  fullname: Beerli, Peter
– sequence: 5
  givenname: Hugo O.
  orcidid: 0000-0003-2159-5667
  surname: Valdivia
  fullname: Valdivia, Hugo O.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/35605021$$D View this record in MEDLINE/PubMed
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crossref_primary_10_1038_s41467_023_44085_2
crossref_primary_10_1371_journal_pntd_0012113
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DocumentTitleAlternate Population genetics of Leishmania (Viannia) braziliensis in Peru
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Current address: Faculty of Medicine and Health Sciences, University of Antwerp, Antwerp, Belgium
The authors have declared that no competing interests exist.
ORCID 0000-0003-0033-6770
0000-0003-0947-5451
0000-0002-4193-8017
0000-0002-3379-4869
0000-0003-2159-5667
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  publication-title: História, Ciências, Saúde-Manguinhos.
  doi: 10.1590/S0104-59702003000300004
– volume: 112
  year: 2017
  ident: pntd.0010374.ref048
  article-title: First description of Leishmania (viannia) infection in Evandromyia saulensis, pressatia sp. and Trichophoromyia auraensis (psychodidae: Phlebotominae) in a transmission area of cutaneous leishmaniasis in Acre State, amazon basin, Brazil.
  publication-title: Mem Inst Oswaldo Cruz
– volume: 18
  start-page: 48
  year: 2013
  ident: pntd.0010374.ref011
  article-title: Spatial distribution and population genetics of Leishmania infantum genotypes in São Paulo State, Brazil, employing multilocus microsatellite typing directly in dog infected tissues
  publication-title: Infect Genet Evol
  doi: 10.1016/j.meegid.2013.04.031
SSID ssj0059581
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Snippet Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military forces deployed...
Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military...
L . (V . ) braziliensis is widespread in the Peruvian jungle region. In this region, the departments of Cusco and Madre de Dios account for a large number of...
Background Human cutaneous leishmaniasis caused by Leishmania (Viannia) braziliensis is highly prevalent in the Peruvian jungle, where it affects military...
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StartPage e0010374
SubjectTerms Biological diversity
Biology and Life Sciences
Clusters
Colonization
Cutaneous leishmaniasis
Distribution
Earth Sciences
Ecology and Environmental Sciences
Economic activities
Equilibrium
Evaluation
Gene polymorphism
Genetic aspects
Genetic diversity
Genetic variation
Geographical distribution
Human subjects
Humans
Inbreeding
Leishmania
Leishmania braziliensis - genetics
Leishmaniasis, Cutaneous - parasitology
Linkage disequilibrium
Markers
Microsatellite Repeats
Microsatellites
Migration
Parasites
Parasitic diseases
People and places
Peru - epidemiology
Polymorphism
Polymorphism, Genetic
Population
Population biology
Population genetics
Population structure
Subpopulations
Tropical diseases
Vector-borne diseases
Vectors
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Title Genetic diversity and population structure of Leishmania (Viannia) braziliensis in the Peruvian jungle
URI https://www.ncbi.nlm.nih.gov/pubmed/35605021
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http://dx.doi.org/10.1371/journal.pntd.0010374
Volume 16
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