Asymmetric introgression between the M and S forms of the malaria vector, Anopheles gambiae, maintains divergence despite extensive hybridization

Abstract

The suggestion that genetic divergence can arise and/or be maintained in the face of gene flow has been contentious since first proposed. This controversy and a rarity of good examples have limited our understanding of this process. Partially reproductively isolated taxa have been highlighted as offering unique opportunities for identifying the mechanisms underlying divergence with gene flow. The African malaria vector, Anopheles gambiae s.s., is widely regarded as consisting of two sympatric forms, thought by many to represent incipient species, the M and S molecular forms. However, there has been much debate about the extent of reproductive isolation between M and S, with one view positing that divergence may have arisen and is being maintained in the presence of gene flow, and the other proposing a more advanced speciation process with little realized gene flow because of low hybrid fitness. These hypotheses have been difficult to address because hybrids are typically rare (<1%). Here, we assess samples from an area of high hybridization and demonstrate that hybrids are fit and responsible for extensive introgression. Nonetheless, we show that strong divergent selection at a subset of loci combined with highly asymmetric introgression has enabled M and S to remain genetically differentiated despite extensive gene flow. We propose that the extent of reproductive isolation between M and S varies across West Africa resulting in a 'geographic mosaic of reproductive isolation'; a finding which adds further complexity to our understanding of divergence in this taxon and which has considerable implications for transgenic control strategies.

Fig. 1

Distribution of molecular forms in Guinea-Bissau. Land cover is coloured according to the University of Maryland Land Cover Scheme of 2008 remote sensing data

Fig. 2

Clustering analyses of SNP genotype data for M (N=45), S (N=170) and hybrid form samples (H, N=108) as defined by Scott diagnostic SNP⁵⁸¹. a) PCoA analysis identified three clusters: 1 - all M samples; 2 – approximately half of the hybrids: 3 - all S samples and the remaining hybrids. b) Clustering using STRUCTURE. Individuals are represented by columns, with colours showing the proportion of their genome assigned to the different clusters. Shown is the most likely number of clusters, K=2, (Fig. S1a, Supplementary Information), which demonstrates that M and S form largely independent clusters with hybrids exhibiting either an admixed M-S or largely S genotype. Similar results were found at higher K values (Fig. S1b, Supplementary Information)

Fig. 3

The proportion of S ancestry in hybrids as identified by STRUCTURE. Plotted are the S ancestry proportions of field collected hybrids (x), the values of which have been ranked, and then plotted against those ranks. The shaded area depicts the range of S ancestry proportions expected for F₁ hybrids based on assessments of simulated hybrids, and dotted lines the range for SxF_1+n and MxF_1+n backcrosses (Table S4, Supplementary Information).