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

Abstract

The M and S forms of Anopheles gambiae have been the focus of intense study by malaria researchers and evolutionary biologists interested in ecological speciation. Divergence occurs at three discrete islands in genomes that are otherwise nearly identical. An "islands of speciation" model proposes that diverged regions contain genes that are maintained by selection in the face of gene flow. An alternative "incidental island" model maintains that gene flow between M and S is effectively zero and that divergence islands are unrelated to speciation. A "divergence island SNP" assay was used to explore the spatial and temporal distributions of hybrid genotypes. Results revealed that hybrid individuals occur at frequencies ranging between 5% and 97% in every population examined. A temporal analysis revealed that assortative mating is unstable and periodically breaks down, resulting in extensive hybridization. Results suggest that hybrids suffer a fitness disadvantage, but at least some hybrid genotypes are viable. Stable introgression of the 2L speciation island occurred at one site following a hybridization event.reproductive isolation | population structure | Anopheles coluzzii

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

“…In Selenkenyi, only 2 out of 280 backcrossed individuals were homozygous-susceptible (+/+), a significant deficiency relative to expected (N exp = 24.4; P < 0.0001 using randomization goodness of fit with 10,000 replicates). Lee et al (5) showed that an earlier hybridization episode in 2002, before the introduction of ITNs in Selenkenyi, was followed by strong selection against hybrids, presumably related to ecological maladaptation or decreased mating success. Thus, it appears that the introduction of L1014F in the presence of insecticide pressure was a key factor that allowed hybrids to overcome an intrinsic selective disadvantage and backcross with the A. coluzzii parental population, contributing to gene flow between the two species.…”

“…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).…”

“…A longitudinal survey conducted as part of that study revealed temporal as well as spatial heterogeneity, with long periods of strong RI interrupted by episodes of hybridization (i.e., abrupt appearance of F 1 genotypes), followed by the disappearance of hybrid genotypes and reestablishment of disequilibrium. A different pattern emerged after an episode of hybridization that occurred in 2006, when SNPs on the X and third chromosome did return to high linkage disequilibrium (LD; R 2 > 0.8), but chromosome 2 SNPs, previously fixed in A. gambiae, introgressed into the A. coluzzii genome (5).…”

“…The knockdown resistance SNP, L1014F (11), in the para voltage-gated sodium channel gene (kdr) is located ∼2.4 Mbp from the 2L centromere and within the introgressed region identified by Lee et al (5). The L1014F SNP is thought to have arisen in West African A. gambiae populations (12) and confers target site resistance to dichlorodiphenyltrichloroethane (DDT) and pyrethroid insecticides (11,13).…”

Plasmodium falciparum infection rates for some Anopheles spp. from Guinea-Bissau, West Africa

“…The Senegal study site at Dielmo and nine of our study sites were proximal (<50km) to the Atlantic Ocean, while Mali is a land-locked country at least 500km away from the Atlantic Ocean. Therefore, the discrepancy among studies may be due to climatic and environmental pressure on the different genetic backgrounds of A. gambiae observed in this area of West Africa ( Lee et al , 2013). More robust sampling over a larger number of collection sites would help in confirming this trend.…”