Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America

ABSTRACT The malaria parasite, Plasmodium falciparum, was introduced into Hispaniola and other regions of the Americas through the slave trade spanning the 16th through the 19th centuries. During this period, more than 12 million Africans were brought across the Atlantic to the Caribbean and other r...

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Autores principales:	Massimiliano S. Tagliamonte, Charles A. Yowell, Maha A. Elbadry, Jacques Boncy, Christian P. Raccurt, Bernard A. Okech, Erica M. Goss, Marco Salemi, John B. Dame
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Haiti Plasmodium falciparum adaptive mutations evolutionary biology malaria phylogenetics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0000e17190e246e6b2621356f3ffcae1
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spelling	oai:doaj.org-article:0000e17190e246e6b2621356f3ffcae12021-11-15T15:30:58ZGenetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America10.1128/mSphere.00937-202379-5042https://doaj.org/article/0000e17190e246e6b2621356f3ffcae12020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00937-20https://doaj.org/toc/2379-5042ABSTRACT The malaria parasite, Plasmodium falciparum, was introduced into Hispaniola and other regions of the Americas through the slave trade spanning the 16th through the 19th centuries. During this period, more than 12 million Africans were brought across the Atlantic to the Caribbean and other regions of the Americas. Since malaria is holoendemic in West Africa, a substantial percentage of these individuals carried the parasite. St. Domingue on Hispaniola, now modern-day Haiti, was a major port of disembarkation, and malaria is still actively transmitted there. We undertook a detailed study of the phylogenetics of the Haitian parasites and those from Colombia and Peru utilizing whole-genome sequencing. Principal-component and phylogenetic analyses, based upon single nucleotide polymorphisms (SNPs) in protein coding regions, indicate that, despite the potential for millions of introductions from Africa, the Haitian parasites share an ancestral relationship within a well-supported monophyletic clade with parasites from South America, while belonging to a distinct lineage. This result, in stark contrast to the historical record of parasite introductions, is best explained by a severe population bottleneck experienced by the parasites introduced into the Americas. Here, evidence is presented for targeted selection of rare African alleles in genes which are expressed in the mosquito stages of the parasite’s life cycle. These genetic markers support the hypothesis that the severe population bottleneck was caused by the required adaptation of the parasite to transmission by new definitive hosts among the Anopheles (Nyssorhynchus) spp. found in the Caribbean and South America. IMPORTANCE Historical data suggest that millions of P. falciparum parasite lineages were introduced into the Americas during the trans-Atlantic slave trade, which would suggest a paraphyletic origin of the extant isolates in the Western Hemisphere. Our analyses of whole-genome variants show that the American parasites belong to a well-supported monophyletic clade. We hypothesize that the required adaptation to American vectors created a severe bottleneck, reducing the effective introduction to a few lineages. In support of this hypothesis, we discovered genes expressed in the mosquito stages of the life cycle that have alleles with multiple, high-frequency or fixed, nonsynonymous mutations in the American populations which are rarely found in African isolates. These alleles appear to be in gene products critical for transmission through the anopheline vector. Thus, these results may inform efforts to develop novel transmission-blocking vaccines by identifying parasite proteins functionally interacting with the vector that are important for successful transmission. Further, to the best of our knowledge, these are the first whole-genome data available from Haitian P. falciparum isolates. Defining the genome of these parasites provides genetic markers useful for mapping parasite populations and monitoring parasite movements/introductions.Massimiliano S. TagliamonteCharles A. YowellMaha A. ElbadryJacques BoncyChristian P. RaccurtBernard A. OkechErica M. GossMarco SalemiJohn B. DameAmerican Society for MicrobiologyarticleHaitiPlasmodium falciparumadaptive mutationsevolutionary biologymalariaphylogeneticsMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Haiti Plasmodium falciparum adaptive mutations evolutionary biology malaria phylogenetics Microbiology QR1-502
spellingShingle	Haiti Plasmodium falciparum adaptive mutations evolutionary biology malaria phylogenetics Microbiology QR1-502 Massimiliano S. Tagliamonte Charles A. Yowell Maha A. Elbadry Jacques Boncy Christian P. Raccurt Bernard A. Okech Erica M. Goss Marco Salemi John B. Dame Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
description	ABSTRACT The malaria parasite, Plasmodium falciparum, was introduced into Hispaniola and other regions of the Americas through the slave trade spanning the 16th through the 19th centuries. During this period, more than 12 million Africans were brought across the Atlantic to the Caribbean and other regions of the Americas. Since malaria is holoendemic in West Africa, a substantial percentage of these individuals carried the parasite. St. Domingue on Hispaniola, now modern-day Haiti, was a major port of disembarkation, and malaria is still actively transmitted there. We undertook a detailed study of the phylogenetics of the Haitian parasites and those from Colombia and Peru utilizing whole-genome sequencing. Principal-component and phylogenetic analyses, based upon single nucleotide polymorphisms (SNPs) in protein coding regions, indicate that, despite the potential for millions of introductions from Africa, the Haitian parasites share an ancestral relationship within a well-supported monophyletic clade with parasites from South America, while belonging to a distinct lineage. This result, in stark contrast to the historical record of parasite introductions, is best explained by a severe population bottleneck experienced by the parasites introduced into the Americas. Here, evidence is presented for targeted selection of rare African alleles in genes which are expressed in the mosquito stages of the parasite’s life cycle. These genetic markers support the hypothesis that the severe population bottleneck was caused by the required adaptation of the parasite to transmission by new definitive hosts among the Anopheles (Nyssorhynchus) spp. found in the Caribbean and South America. IMPORTANCE Historical data suggest that millions of P. falciparum parasite lineages were introduced into the Americas during the trans-Atlantic slave trade, which would suggest a paraphyletic origin of the extant isolates in the Western Hemisphere. Our analyses of whole-genome variants show that the American parasites belong to a well-supported monophyletic clade. We hypothesize that the required adaptation to American vectors created a severe bottleneck, reducing the effective introduction to a few lineages. In support of this hypothesis, we discovered genes expressed in the mosquito stages of the life cycle that have alleles with multiple, high-frequency or fixed, nonsynonymous mutations in the American populations which are rarely found in African isolates. These alleles appear to be in gene products critical for transmission through the anopheline vector. Thus, these results may inform efforts to develop novel transmission-blocking vaccines by identifying parasite proteins functionally interacting with the vector that are important for successful transmission. Further, to the best of our knowledge, these are the first whole-genome data available from Haitian P. falciparum isolates. Defining the genome of these parasites provides genetic markers useful for mapping parasite populations and monitoring parasite movements/introductions.
format	article
author	Massimiliano S. Tagliamonte Charles A. Yowell Maha A. Elbadry Jacques Boncy Christian P. Raccurt Bernard A. Okech Erica M. Goss Marco Salemi John B. Dame
author_facet	Massimiliano S. Tagliamonte Charles A. Yowell Maha A. Elbadry Jacques Boncy Christian P. Raccurt Bernard A. Okech Erica M. Goss Marco Salemi John B. Dame
author_sort	Massimiliano S. Tagliamonte
title	Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
title_short	Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
title_full	Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
title_fullStr	Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
title_full_unstemmed	Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America
title_sort	genetic markers of adaptation of <named-content content-type="genus-species">plasmodium falciparum</named-content> to transmission by american vectors identified in the genomes of parasites from haiti and south america
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/0000e17190e246e6b2621356f3ffcae1
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Genetic Markers of Adaptation of <named-content content-type="genus-species">Plasmodium falciparum</named-content> to Transmission by American Vectors Identified in the Genomes of Parasites from Haiti and South America

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