Population genetic structure and adaptation of malaria parasites on the edge of endemic distribution

Craig W. Duffy*, Hampate Ba, Samuel Assefa, Ambroise D. Ahouidi, Yacine B. Deh, Abderahmane Tandia, Freja C.M. Kirsebom, Dominic P. Kwiatkowski, David J. Conway

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

21 Citations (Scopus)

Abstract

To determine whether the major human malaria parasite Plasmodium falciparum exhibits fragmented population structure or local adaptation at the northern limit of its African distribution where the dry Sahel zone meets the Sahara, samples were collected from diverse locations within Mauritania over a range of ~1000 km. Microsatellite genotypes were obtained for 203 clinical infection samples from eight locations, and Illumina paired-end sequences were obtained to yield high coverage genomewide single nucleotide polymorphism (SNP) data for 65 clinical infection samples from four locations. Most infections contained single parasite genotypes, reflecting low rates of transmission and superinfection locally, in contrast to the situation seen in population samples from countries further south. A minority of infections shared related or identical genotypes locally, indicating some repeated transmission of parasite clones without recombination. This caused some multilocus linkage disequilibrium and local divergence, but aside from the effect of repeated genotypes there was minimal differentiation between locations. Several chromosomal regions had elevated integrated haplotype scores (|iHS|) indicating recent selection, including those containing drug resistance genes. A genomewide FST scan comparison with previous sequence data from an area in West Africa with higher infection endemicity indicates that regional gene flow prevents genetic isolation, but revealed allele frequency differentiation at three drug resistance loci and an erythrocyte invasion ligand gene. Contrast of extended haplotype signatures revealed none to be unique to Mauritania. Discrete foci of infection on the edge of the Sahara are genetically highly connected to the wider continental parasite population, and local elimination would be difficult to achieve without very substantial reduction in malaria throughout the region.

Original languageEnglish
Pages (from-to)2880-2894
Number of pages15
JournalMolecular Ecology
Volume26
Issue number11
DOIs
Publication statusPublished - Jun 2017
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful to all patients with malaria who participated in the study, as well as staff at each of the hospitals and health centres in Mauritania who supported the sample collection. We are grateful to Lindsay Stewart, Bronwyn MacInnis, Vikki Cornelius, Eleanor Drury, Daniel Mead and colleagues who helped with sample processing and transport, as well as processing for genome sequencing and data archiving. This research was funded by MRC grant G1100123 and ERC grant AdG-2011-294428, with additional support for genome sequencing in collaboration with the MalariaGEN consortium (www.malariagen.net) funded by MRC grant G0600718 and Wellcome Trust grant 090770/Z/09/Z.

Publisher Copyright:
© 2017 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd

Keywords

  • adaptation
  • biomedicine
  • disease biology
  • ecological genetics
  • genomics/proteomics
  • microbial biology

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