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 has 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 realised gene flow due to 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 hybridisation 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 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.

Physiological correlates of ecological divergence along an urbanization gradient: differential tolerance to ammonia among molecular forms of the malaria mosquito Anopheles gambiae

“…Asymmetric introgression of maladaptive alleles present in the rural S population into the urban M population may hinder greater phenotypic divergence between the two forms, unless the genes underlying this phenotype are linked to genes controlling reproductive isolation between the two forms—a condition that would favour ecological speciation if ammonia tolerance is adaptive. Asymmetric introgression of M-form nuclear genes into the S-form genome (a pattern opposite to that predicted by our observations) has been demonstrated in Guinea Bissau, a relatively restricted geographical area of high hybridization between the two forms [64,65]. In a similar way, neighbouring demes of the larger M-form metapopulation occurring in forested southern Cameroon [18], connected by dispersal to the Yaounde deme, may introduce maladaptive tolerance alleles if these allochthonous demes do not share the same local adaptation mechanisms of the Yaounde deme.…”

“…Gene flow between the M and S molecular forms is strongly reduced but—apparently—not nil [64-66]. Asymmetric introgression of maladaptive alleles present in the rural S population into the urban M population may hinder greater phenotypic divergence between the two forms, unless the genes underlying this phenotype are linked to genes controlling reproductive isolation between the two forms—a condition that would favour ecological speciation if ammonia tolerance is adaptive.…”

Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae

“…2 K-N and SI Appendix, Fig. S7 A-D), presumably due to a strong asymmetry in assortative mating (22). Loss of the chromosome 2L island of divergence was observed in populations at Bioko and Selinkenyi (Fig.…”

Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets

“…Initially described as the M and S molecular forms, they are now recognized species, designated Anopheles coluzzii and Anopheles gambiae, respectively (1). The two species exhibit varying degrees of reproductive isolation (RI) across their range (2)(3)(4)(5)(6), and recent studies provide strong evidence for reduced hybrid fitness in nature (5).…”