Adaptive Potential of Hybridization among Malaria Vectors: Introgression at the Immune Locus TEP1 between Anopheles coluzzii and A. gambiae in 'Far-West' Africa

PLoS One. 2015 Jun 5;10(6):e0127804. doi: 10.1371/journal.pone.0127804. eCollection 2015.

Abstract

"Far-West" Africa is known to be a secondary contact zone between the two major malaria vectors Anopheles coluzzii and A. gambiae. We investigated gene-flow and potentially adaptive introgression between these species along a west-to-east transect in Guinea Bissau, the putative core of this hybrid zone. To evaluate the extent and direction of gene flow, we genotyped site 702 in Intron-1 of the para Voltage-Gated Sodium Channel gene, a species-diagnostic nucleotide position throughout most of A. coluzzii and A. gambiae sympatric range. We also analyzed polymorphism in the thioester-binding domain (TED) of the innate immunity-linked thioester-containing protein 1 (TEP1) to investigate whether elevated hybridization might facilitate the exchange of variants linked to adaptive immunity and Plasmodium refractoriness. Our results confirm asymmetric introgression of genetic material from A. coluzzii to A. gambiae and disruption of linkage between the centromeric "genomic islands" of inter-specific divergence. We report that A. gambiae from the Guinean hybrid zone possesses an introgressed TEP1 resistant allelic class, found exclusively in A. coluzzii elsewhere and apparently swept to fixation in West Africa (i.e. Mali and Burkina Faso). However, no detectable fixation of this allele was found in Guinea Bissau, which may suggest that ecological pressures driving segregation between the two species in larval habitats in this region may be different from those experienced in northern and more arid parts of the species' range. Finally, our results also suggest a genetic subdivision between coastal and inland A. gambiae Guinean populations and provide clues on the importance of ecological factors in intra-specific differentiation processes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity
  • Africa, Western
  • Alleles
  • Amino Acid Sequence
  • Animals
  • Anopheles / genetics*
  • Anopheles / growth & development
  • Anopheles / parasitology
  • Gene Flow
  • Genes, Insect
  • Genetic Loci
  • Genetics, Population
  • Genotype
  • Guinea-Bissau
  • Haplotypes
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Linkage Disequilibrium
  • Molecular Sequence Data
  • Plasmodium / physiology
  • Polymorphism, Single Nucleotide
  • Sequence Alignment

Substances

  • Insect Proteins
  • TEP1 protein, Anopheles gambiae

Grants and funding

This work was supported by the European Union’s INFRAVEC project (Grant agreement no. 228421, under FP7 program) to AdT and JP; FCT Portugal/FEDER (through program COMPETE) co-funds (PTDC/BIA-EVF/120407/2010); AWARD 2013 grant by 'Sapienza' Università di Roma to AdT, MIUR-FIRB “Futuro in Ricerca 2010” grant to BC (Grant N° RBFR106NTE).