Host Switch Leads to Emergence of Plasmodium vivax Malaria in Humans

Mu, Jianbing; Joy, Deirdre A.; Duan, Junhui; Huang, Yaming; Carlton, Jane M.; Walker, John C.; Barnwell, John W.; Beerli, Peter; Charleston, Michael A.; Pybus, Oliver G.; Su, Xin-zhuan

doi:10.1093/molbev/msi160

Cited by 196 publications

(247 citation statements)

References 39 publications

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“…Our T MRCA estimates of human-specific P.vivax sequences are 70-250 kya (S12 Table), consistent with previous estimates (50-500 kya, [42,43,89]). As the T MRCA of human-specific P.vivax is estimated to be before or overlapping the T MRCA of FY Ã O, this is consistent with the hypothesis of P.vivax being the selective agent responsible for the rise of FY Ã O in Africa.…”

Section: Fy*o and Fy*a Mutations And P Vivaxsupporting

confidence: 90%

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Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

McManus

Taravella

Henn

et al. 2016

Preprint

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The human DARC (Duffy antigen receptor for chemokines) gene encodes a membranebound chemokine receptor crucial for the infection of red blood cells by Plasmodium vivax, a major causative agent of malaria. Of the three major allelic classes segregating in human populations, the FY*O allele has been shown to protect against P. vivax infection and is at near fixation in sub-Saharan Africa, while FY*B and FY*A are common in Europe and Asia, respectively. Due to the combination of strong geographic differentiation and association with malaria resistance, DARC is considered a canonical example of positive selection in humans. Despite this, details of the timing and mode of selection at DARC remain poorly understood. Here, we use sequencing data from over 1,000 individuals in twenty-one human populations, as well as ancient human genomes, to perform a fine-scale investigation of the evolutionary history of DARC. We estimate the time to most recent common ancestor (T MRCA ) of the most common FY*O haplotype to be 42 kya (95% CI: 34-49 kya). We infer the FY*O null mutation swept to fixation in Africa from standing variation with very low initial frequency (0.1%) and a selection coefficient of 0.043 (95% CI:0.011-0.18), which is among the strongest estimated in the human genome. We estimate the T MRCA of the FY*A mutation in non-Africans to be 57 kya (95% CI: 48-65 kya) and infer that, prior to the sweep of FY*O, all three alleles were segregating in Africa, as highly diverged populations from Asia and 6 ¼Khomani San hunter-gatherers share the same FY*A haplotypes. We test multiple models of admixture that may account for this observation and reject recent Asian or European admixture as the cause.

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Section: Fy*o and Fy*a Mutations And P Vivaxsupporting

confidence: 90%

“…We assumed a star-like phylogeny and used the same pairwise differences equation as in the FY Ã O/FY Ã A estimates to calculate the T MRCA of each P.vivax gene. We assumed a mutation rate of 5.07 Ã 10 −9 basepairs per generation and a generation time of 1 year [89]. Dashed line indicates position of the DARC gene.…”

Section: Population Structure Analysesmentioning

confidence: 99%

Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

McManus

Taravella

Henn

et al. 2016

Preprint

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“…What are the links between the sylvatic and the human P. vivax clades? Considering that the P. vivax lineage is of Asian origin (29), Fig. 3 outlines four different possible scenarios.…”

Section: Discussionmentioning

confidence: 99%

“…Blood tests showed thrombocytopenia (platelet count, 105 Giga/L), no anemia Network was built using 226 P. vivax sequences (218 previously published (3,11,29), and eight samples from this work). (B) The 18S gene.…”

Section: Phylogenetic and Genetic Analyses Of P Vivax-like Parasitesmentioning

confidence: 99%

Diversity, host switching and evolution of Plasmodium vivax infecting African great apes

Prugnolle

Rougeron

Becquart

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

119

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Plasmodium vivax is considered to be absent from Central and West Africa because of the protective effect of Duffy negativity. However, there are reports of persons returning from these areas infected with this parasite and observations suggesting the existence of transmission. Among the possible explanations for this apparent paradox, the existence of a zoonotic reservoir has been proposed. May great apes be this reservoir? We analyze the mitochondrial and nuclear genetic diversity of P. vivax parasites isolated from great apes in Africa and compare it to parasites isolated from travelers returning from these regions of Africa, as well as to human isolates distributed all over the world. We show that the P. vivax sequences from parasites of great apes form a clade genetically distinct from the parasites circulating in humans. We show that this clade's parasites can be infectious to humans by describing the case of a traveler returning from the Central African Republic infected with one of them. The relationship between this P. vivax clade in great apes and the human isolates is discussed.emergence | transfer | malaria | sylvatic | origin

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“…However, the high prevalence in sub-Saharan Africa of Duffy negativity (absence of the Duffy blood group antigen) that protects against P. vivax infection has been interpreted as evidence of the African origin of P. vivax (4)(5)(6). Most recently, phylogenetic and biogeographical evidence has been advanced supporting a Southeast Asia origin (7)(8)(9).…”

mentioning

confidence: 99%

Plasmodium vivax : Recent world expansion and genetic identity to Plasmodium simium

Lim

Tazi

Ayala

2005

Proc. Natl. Acad. Sci. U.S.A.

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Plasmodium vivax causes the most geographically widespread human malaria, accounting annually for 70 -80 million clinical cases throughout the tropical and subtropical regions of the world's continents. We have analyzed the DNA sequences of the Csp (circumsporozoite protein) gene in 24 geographically representative strains of P. vivax and 2 of P. simium, which parasitizes several species of New World monkeys. The Csp sequences are of two types, VK210 and VK247, which differ by three diagnostic amino acid replacements, one in each of the 5 and 3 terminal regions [5 nonrepeat (NR) and 3 NR] of the gene and in an insertion sequence that precedes the 3 NR region. The central region of the gene consists of Ϸ38 repetitive ''motifs,'' which are alternatively four and five amino acids long, which also are diagnostically different between the VK210 and VK247 types. There are very few synonymous substitutions within and between the two types of strains, which we hypothesize reflects that the worldwide spread of P. vivax is very recent. The two P. simium Csp sequences belong one to each of the two VK types and are genetically indistinguishable from the corresponding P. vivax strains, suggesting that at least two host transfers have occurred between humans and New World monkeys. We exclude as unlikely the possibility that the two types of sequences could have independently arisen in humans and platyrrhines by natural selection. There are reasons favoring each of the two possible directions of host transfer between humans and monkeys.circumsporozoite protein ͉ clonal theory ͉ Plasmodium population structure ͉ host-parasite interactions ͉ malaria M alaria's human toll is appalling: 300-500 million clinical cases and 1-3 million deaths per year. Plasmodium falciparum accounts for 80% of human malaria's morbidity and mortality, mostly in sub-Saharan Africa. Most geographically widespread and prevalent in some regions is Plasmodium vivax, which accounts annually for 70-80 million clinical cases across much of the tropics and subtropics of the world.The evolutionary origin of P. vivax has been placed by some authors in Southeast Asia (1-3). However, the high prevalence in sub-Saharan Africa of Duffy negativity (absence of the Duffy blood group antigen) that protects against P. vivax infection has been interpreted as evidence of the African origin of P. vivax (4-6). Most recently, phylogenetic and biogeographical evidence has been advanced supporting a Southeast Asia origin (7-9).Recent investigations have shown a scarcity of selectively neutral genetic polymorphisms in P. vivax (8,10,11), which is consistent with a recent world expansion of P. vivax as a human parasite. The discovery that the platyrrhine parasite P. simium is genetically indistinguishable from P. vivax (2,7,8) manifests that a host transfer between humans and New World monkeys has happened in very recent evolutionary times.The circumsporozoite protein (CSP) has been extensively studied in P. falciparum and other Plasmodium species because of its immune significan...

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Host Switch Leads to Emergence of Plasmodium vivax Malaria in Humans

Cited by 196 publications

References 39 publications

Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

Diversity, host switching and evolution of Plasmodium vivax infecting African great apes

Plasmodium vivax : Recent world expansion and genetic identity to Plasmodium simium

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