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

Isabelle Morlais,François Rousset,Zeinab Annan,Didier Fontenille,Sandrine E Nsango,Parfait H Awono-Ambene,Luc Abate,Antoine Berry,Anna Cohuet,Majoline T Tchioffo,Wilson Toussile

doi:10.1371/journal.pone.0123777

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.

Highlights

Plasmodium falciparum transmission relies on its successful development within the mosquito vector where fertilization occurs
Multiple genotypes are generally found within a single parasite isolate and the complexity of malaria infections has often impeded genetic studies on P. falciparum [5,6]
We have modeled the mosquito infection according to gametocyte variables to provide insights into the transmission of P. falciparum genotypes in the field

Summary

Introduction

Plasmodium falciparum transmission relies on its successful development within the mosquito vector where fertilization occurs. Studies on malaria parasite genetic structure have revealed different mating patterns in multiple epidemiological settings. Large deviations from panmixia were observed in malaria endemic areas and it has been argued that self-fertilization would favor transmission of better adapted strains of parasites. Multiple genotypes are generally found within a single parasite isolate and the complexity of malaria infections has often impeded genetic studies on P. falciparum [5,6]. Modeling malaria transmission is crucial to understand the evolution of parasites and vectors and to predict the long-term impact of global control measures. The results show how the genetic composition of the gametocyte population impacts on the infection success of the mosquito and describe the important role of the insect vector in maintaining the parasite genetic diversity

Ethics statement

Results

Discussion