Plasmodium falciparum mating patterns and mosquito infectivity of natural isolates of gametocytes

PLoS One. 2015 Apr 14;10(4):e0123777. doi: 10.1371/journal.pone.0123777. eCollection 2015.

Abstract

Plasmodium falciparum infections in malaria endemic areas often harbor multiple clones of parasites. However, the transmission success of the different genotypes within the mosquito vector has remained elusive so far. The genetic diversity of malaria parasites was measured by using microsatellite markers in gametocyte isolates from 125 asymptomatic carriers. For a subset of 49 carriers, the dynamics of co-infecting genotypes was followed until their development within salivary glands. Also, individual oocysts from midguts infected with blood from 9 donors were genotyped to assess mating patterns. Multiplicity of infection (MOI) was high both in gametocyte isolates and sporozoite populations, reaching up to 10 genotypes. Gametocyte isolates with multiple genotypes gave rise to lower infection prevalence and intensity. Fluctuations of genotype number occurred during the development within the mosquito and sub-patent genotypes, not detected in gametocyte isolates, were identified in the vector salivary glands. The inbreeding coefficient Fis was positively correlated to the oocyst loads, suggesting that P. falciparum parasites use different reproductive strategies according to the genotypes present in the gametocyte isolate. The number of parasite clones within an infection affects the transmission success and the mosquito has an important role in maintaining P. falciparum genetic diversity. Our results emphasize the crucial importance of discriminating between the different genotypes within an infection when studying the A. gambiae natural resistance to P. falciparum, and the need to monitor parasite diversity in areas where malaria control interventions are implemented.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anopheles / parasitology*
  • Child
  • Child, Preschool
  • DNA, Protozoan / chemistry
  • DNA, Protozoan / isolation & purification
  • DNA, Protozoan / metabolism
  • Female
  • Genetic Variation
  • Genotype
  • Humans
  • Insect Vectors / parasitology
  • Malaria, Falciparum / parasitology
  • Malaria, Falciparum / pathology
  • Microsatellite Repeats / genetics
  • Oocysts / parasitology
  • Plasmodium falciparum / genetics*
  • Plasmodium falciparum / growth & development
  • Plasmodium falciparum / physiology
  • Reproduction
  • Sporozoites / metabolism

Substances

  • DNA, Protozoan

Grants and funding

This work was supported by the Institut de Recherche pour le Développement (scholarships awarded to SEN and WT), the Institut de Médecine et d'Epidémiologie Appliquée (IMEA-AO-07 to AB), the Agence Nationale de la Recherche (ANR-11-BSV7-009-01 to IM), and the European Union Seventh Framework Programme (GA242095-EviMalaR to DF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.