Patterns of selection on Plasmodium falciparum erythrocyte-binding antigens after the colonization of the New World

Authors

  • Erhan Yalcindag,

    Corresponding author
    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    2. Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic
    Search for more papers by this author
    • E.Y. and V.R. Contributed equally to this work.
  • Virginie Rougeron,

    Corresponding author
    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    2. Centre International de Recherches Médicales de Franceville (CIRMF), Franceville, Gabon
    Search for more papers by this author
    • E.Y. and V.R. Contributed equally to this work.
  • Eric Elguero,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Céline Arnathau,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Patrick Durand,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Sylvain Brisse,

    1. Institut Pasteur, Plate-forme Génotypage des Pathogènes et Santé Publique, Paris, France
    Search for more papers by this author
  • Laure Diancourt,

    1. Institut Pasteur, Plate-forme Génotypage des Pathogènes et Santé Publique, Paris, France
    Search for more papers by this author
  • Agnes Aubouy,

    1. Institut de Recherche pour le Développement (IRD), UMR152, Université Paul Sabatier, Toulouse, France
    Search for more papers by this author
  • Pierre Becquart,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Umberto D'Alessandro,

    1. Department of Parasitology, Institute of Tropical Medicine, Antwerp, Belgium
    Search for more papers by this author
  • Didier Fontenille,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Dionicia Gamboa,

    1. Instituto de Medicina Tropical Alexander Von Humboldt, Universidad Peruana Cayetano Heredia, Lima, Peru
    Search for more papers by this author
  • Amanda Maestre,

    1. Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquía, Medellín, Colombia
    Search for more papers by this author
  • Didier Ménard,

    1. Molecular Epidemiology Unit, Pasteur Institute of Cambodia, Phnom Penh, Cambodia
    Search for more papers by this author
  • Lise Musset,

    1. Parasitology laboratory, Institut Pasteur de Guyane, Cayenne Cedex, French Guiana
    Search for more papers by this author
  • Oscar Noya,

    1. Centro para Estudios Sobre Malaria, Instituto de Altos Estudios en Salud “Dr. Arnoldo Gabaldón”-INH, Ministerio del Poder Popular para la Salud, Instituto de Medicina Tropical, Universidad Central de Venezuela, Caracas, Venezuela
    Search for more papers by this author
  • Vincent Veron,

    1. INRA, équipe NuMéA, St Pée sur Nivelle, France
    Search for more papers by this author
  • Albina Wide,

    1. Centro para Estudios Sobre Malaria, Instituto de Altos Estudios en Salud “Dr. Arnoldo Gabaldón”-INH, Ministerio del Poder Popular para la Salud, Instituto de Medicina Tropical, Universidad Central de Venezuela, Caracas, Venezuela
    Search for more papers by this author
  • Bernard Carme,

    1. Centre d'Investigation Clinique Epidémiologie Clinique Antilles, Guyane CIC-EC 802, Cayenne General Hospital, Cayenne, French Guiana
    Search for more papers by this author
  • Eric Legrand,

    1. Parasitology laboratory, Institut Pasteur de Guyane, Cayenne Cedex, French Guiana
    Search for more papers by this author
  • Christine Chevillon,

    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
  • Francisco J. Ayala,

    1. Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, USA
    Search for more papers by this author
  • François Renaud,

    Corresponding author
    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    Search for more papers by this author
    • F.P. and F.R. supervised this work.
  • Franck Prugnolle

    Corresponding author
    1. MIVEGEC (Laboratoire Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle), UMR CNRS 5290/IRD 224, Université Montpellier 1, Université Montpellier 2, CHRU de Montpellier, Montpellier, France
    2. Centre International de Recherches Médicales de Franceville (CIRMF), Franceville, Gabon
    Search for more papers by this author
    • F.P. and F.R. supervised this work.

Abstract

Pathogens, which have recently colonized a new host species or new populations of the same host, are interesting models for understanding how populations may evolve in response to novel environments. During its colonization of South America from Africa, Plasmodium falciparum, the main agent of malaria, has been exposed to new conditions in distinctive new human populations (Amerindian and populations of mixed origins) that likely exerted new selective pressures on the parasite's genome. Among the genes that might have experienced strong selective pressures in response to these environmental changes, the eba genes (erythrocyte-binding antigens genes), which are involved in the invasion of the human red blood cells, constitute good candidates. In this study, we analysed, in South America, the polymorphism of three eba genes (eba-140, eba-175, eba-181) and compared it to the polymorphism observed in African populations. The aim was to determine whether these genes faced selective pressures in South America distinct from what they experienced in Africa. Patterns of genetic variability of these genes were compared to the patterns observed at two housekeeping genes (adsl and serca) and 272 SNPs to separate adaptive effects from demographic effects. We show that, conversely to Africa, eba-140 seemed to be under stronger diversifying selection in South America than eba-175. In contrast, eba-181 did not show any sign of departure from neutrality. These changes in the patterns of selection on the eba genes could be the consequence of changes in the host immune response, the host receptor polymorphisms and/or the ability of the parasite to silence or express differentially its invasion proteins.

Ancillary