Abstract

Impacts of introgressive hybridisation may range from genomic erosion and species collapse to rapid adaptation and speciation but opportunities to study these dynamics are rare. We investigated the extent, causes and consequences of a hybrid zone between Anopheles coluzzii and Anopheles gambiae in Guinea-Bissau, where high hybridisation rates appear to be stable at least since the 1990s. Anopheles gambiae was genetically partitioned into inland and coastal subpopulations, separated by a central region dominated by A. coluzzii. Surprisingly, whole genome sequencing revealed that the coastal region harbours a hybrid form characterised by an A. gambiae-like sex chromosome and massive introgression of A. coluzzii autosomal alleles. Local selection on chromosomal inversions may play a role in this process, suggesting potential for spatiotemporal stability of the coastal hybrid form and providing resilience against introgression of medically-important loci and traits, found to be more prevalent in inland A. gambiae.

Highlights

  • With multiple environmental adaptions[8,9,10]

  • Mutations associated with knockdown resistance to DDT and pyrethroid insecticides have been initially found at much higher frequency in A. gambiae than in A. coluzzii even when the species are sympatric[22]

  • We examined the following hypotheses: (1) The hybrid zone is confined to the coastal region and differentiated from inland regions at chromosomal inversion polymorphisms, which may link to local adaptation; (2) Asymmetric introgression from A. coluzzii to A. gambiae is promoting intraspecific divergence between coastal and inland populations of A. gambiae, potentially leading to radiation of a distinct hybrid form; (3) The establishment of a hybrid form builds the potential for aggregation of medically important mutations and phenotypes

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Summary

Introduction

With multiple environmental adaptions[8,9,10]. following the discovery of fixed differences in ribosomal DNA on the pericentromeric region of chromosome-X, which overlapped only partially with the chromosomal forms, focus shifted from chromosomal to ‘molecular forms’, termed M and S11. A recent laboratory study has demonstrated that the chromosome-X island of divergence is associated with assortative mating between A. coluzzii and A. gambiae[21] confirming this genomic region as a primary candidate location for genes involved in reproductive isolation. These species have shown differences in at least two genes which contribute to medically important phenotypes. The available temporal data is based on a relatively limited number of collections and without accounting for eventual seasonal variations Another possibility is that introgression may be creating a pool of aberrantly high diversity facilitating adaptation to new or marginal niches[2,3]. A significantly higher Plasmodium infection rate was detected in A. gambiae when compared with A. coluzzii and hybrids in coastal Guinea Bissau[42], the potential impact of the hybrid zone on Plasmodium transmission and other traits of medical importance, such as insecticide resistance and host preferences, has received limited attention

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