Adaptive immunity selects against malaria infection blocking mutations

The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely, mutations capable of blocking the more lethal P. falciparum have not succeeded in malarious zones. Here we present an evolutionary-epidemiol...

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Published inPLoS computational biology Vol. 16; no. 10; p. e1008181
Main Authors Penman, Bridget S, Gandon, Sylvain
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 08.10.2020
PLOS
Public Library of Science (PLoS)
Subjects
Adaptation
Adaptive immunity
Adaptive Immunity - genetics
Age
Biodiversity and Ecology
Biology and Life Sciences
Blocking
Blood groups
Computational Biology
Costs
Disease transmission
Environmental Sciences
Epidemic models
Epidemiology
Erythrocytes
Evolution, Molecular
Genetic Predisposition to Disease - genetics
Genotype & phenotype
Human populations
Humans
Immunity
Infections
Malaria
Malaria, Falciparum - epidemiology
Malaria, Falciparum - genetics
Malaria, Falciparum - immunology
Malaria, Vivax - epidemiology
Malaria, Vivax - genetics
Malaria, Vivax - immunology
Medicine and Health Sciences
Models, Genetic
Mortality
Mutation
Mutation - genetics
Parasites
Pathogens
Physiological aspects
Plasmodium falciparum - immunology
Plasmodium vivax - immunology
Population
Populations
Success
Vector-borne diseases
Virulence
Indonesia
Online AccessGet full text

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Abstract The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely, mutations capable of blocking the more lethal P. falciparum have not succeeded in malarious zones. Here we present an evolutionary-epidemiological model of malaria which demonstrates that if adaptive immunity against the most virulent effects of malaria is gained rapidly by the host, mutations which prevent infection per se are unlikely to succeed. Our results (i) explain the rarity of strain-transcending P. falciparum infection blocking adaptations in humans; (ii) make the surprising prediction that mutations which block P. falciparum infection are most likely to be found in populations experiencing low or infrequent malaria transmission, and (iii) predict that immunity against some of the virulent effects of P. vivax malaria may be built up over the course of many infections.
AbstractList The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely, mutations capable of blocking the more lethal P . falciparum have not succeeded in malarious zones. Here we present an evolutionary-epidemiological model of malaria which demonstrates that if adaptive immunity against the most virulent effects of malaria is gained rapidly by the host, mutations which prevent infection per se are unlikely to succeed. Our results (i) explain the rarity of strain-transcending P . falciparum infection blocking adaptations in humans; (ii) make the surprising prediction that mutations which block P . falciparum infection are most likely to be found in populations experiencing low or infrequent malaria transmission, and (iii) predict that immunity against some of the virulent effects of P . vivax malaria may be built up over the course of many infections. Malaria has profoundly influenced human evolution. However, humans have adapted to two major malaria parasites, Plasmodium falciparum and Plasmodium vivax , by strikingly different strategies. The Duffy negative blood group impairs P . vivax entry to red blood cells and reduces the chance of becoming infected. No equivalent blocking adaption against P . falciparum has evolved to become widespread, despite the existence of candidate mutations. We show that rapidly gained adaptive immunity to malaria virulence limits the success of infection blocking mutations. This could account for humans’ contrasting adaptations to P . falciparum and P . vivax . Our results highlight the critical role of adaptive immunity in determining how vertebrate hosts evolve in response to pathogen selection, and provide a new framework within which to understand this process.
The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely, mutations capable of blocking the more lethal P. falciparum have not succeeded in malarious zones. Here we present an evolutionary-epidemiological model of malaria which demonstrates that if adaptive immunity against the most virulent effects of malaria is gained rapidly by the host, mutations which prevent infection per se are unlikely to succeed. Our results (i) explain the rarity of strain-transcending P. falciparum infection blocking adaptations in humans; (ii) make the surprising prediction that mutations which block P. falciparum infection are most likely to be found in populations experiencing low or infrequent malaria transmission, and (iii) predict that immunity against some of the virulent effects of P. vivax malaria may be built up over the course of many infections.
Audience Academic
Author Penman, Bridget S
Gandon, Sylvain
AuthorAffiliation University of Chicago, UNITED STATES
2 CEFE, CNRS, University of Montpellier, Paul Valéry University of Montpellier, EPHE, IRD, Montpellier, France
1 Zeeman Institute and School of Life Sciences, University of Warwick, Coventry, United Kingdom
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ContentType Journal Article
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2020 Penman, Gandon. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Snippet The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely,...
The mutation responsible for Duffy negativity, which impedes Plasmodium vivax infection, has reached high frequencies in certain human populations. Conversely,...
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StartPage e1008181
SubjectTerms Adaptation
Adaptive immunity
Adaptive Immunity - genetics
Age
Biodiversity and Ecology
Biology and Life Sciences
Blocking
Blood groups
Computational Biology
Costs
Disease transmission
Environmental Sciences
Epidemic models
Epidemiology
Erythrocytes
Evolution, Molecular
Genetic Predisposition to Disease - genetics
Genotype & phenotype
Human populations
Humans
Immunity
Infections
Malaria
Malaria, Falciparum - epidemiology
Malaria, Falciparum - genetics
Malaria, Falciparum - immunology
Malaria, Vivax - epidemiology
Malaria, Vivax - genetics
Malaria, Vivax - immunology
Medicine and Health Sciences
Models, Genetic
Mortality
Mutation
Mutation - genetics
Parasites
Pathogens
Physiological aspects
Plasmodium falciparum - immunology
Plasmodium vivax - immunology
Population
Populations
Success
Vector-borne diseases
Virulence
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Title Adaptive immunity selects against malaria infection blocking mutations
URI https://www.ncbi.nlm.nih.gov/pubmed/33031369
https://www.proquest.com/docview/2460773098
https://search.proquest.com/docview/2449953806
https://hal.science/hal-03091806
https://pubmed.ncbi.nlm.nih.gov/PMC7544067
https://doaj.org/article/abe0a2f25fc54dd6be35bdb43812ce51
http://dx.doi.org/10.1371/journal.pcbi.1008181
Volume 16
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