Abstract

Ongoing speciation in the most important African malaria vectors gives rise to cryptic populations, which differ remarkably in their behavior, ecology, and capacity to vector malaria parasites. Understanding the population structure and the drivers of genetic differentiation among mosquitoes is crucial for effective disease control because heterogeneity within vector species contributes to variability in malaria cases and allow fractions of populations to escape control efforts. To examine population structure and the potential impacts of recent large‐scale control interventions, we have investigated the genomic patterns of differentiation in mosquitoes belonging to the Anopheles nili group—a large taxonomic group that diverged ~3 Myr ago. Using 4,343 single nucleotide polymorphisms (SNPs), we detected strong population structure characterized by high‐F ST values between multiple divergent populations adapted to different habitats within the Central African rainforest. Delineating the cryptic species within the Anopheles nili group is challenging due to incongruence between morphology, ribosomal DNA, and SNP markers consistent with incomplete lineage sorting and/or interspecific gene flow. A very high proportion of loci are fixed (F ST = 1) within the genome of putative species, which suggests that ecological and/or reproductive barriers are maintained by strong selection on a substantial number of genes.

Highlights

  • One of the principal goals of population genetics is to summarize the genetic similarities and differences between populations (Wright, 1984)

  • The best known mosquito species of the genus Anopheles — which includes all vectors of Plasmodium, the parasite of human malaria — exhibit very complex range-wide population structure due to the combined effects of cryptic speciation, adaptive flexibility and ongoing gene flow (Harbach, 2013; Krzywinski and Besansky, 2003)

  • We have focused on malaria mosquitoes of the An. nili group, whose taxonomy and population structure have been challenging to resolve with low-resolution markers

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Summary

Introduction

One of the principal goals of population genetics is to summarize the genetic similarities and differences between populations (Wright, 1984). Almost all the major malaria vectors of the Afrotropical region belong to large taxonomic groups encompassing multiple incipient species relatively isolated reproductively and geographically from one another (reviewed by Sinka et al 2010; Antonio-Nkondjio and Simard 2013; Coetzee and Koekemoer 2013; Dia et al 2013; Lanzaro and Lee 2013). These characteristics make them promising model systems to study speciation and the processes which contribute to reproductive barriers Single-population models were fitted to allele frequency spectra, and the best model was selected using the lowest likelihood and Akaike Information Criterion as well as visual inspections of residuals

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