Insights into the hybridization occurring between the two molecular forms of the malaria mosquito Anopheles gambiae s.s

Anopheles gambiae s.s., the most important mosquito species transmitting malaria in sub-Saharan Africa, is experiencing an incipient speciation process triggered by human-made environmental changes, which is changing malaria epidemiology. The species is subdivided into two molecular forms, named ‘M’ and ‘S’, defined on rDNA-IGS mutations and distinguished for the M form-specific insertion of a SINE transposable element (~1 Mb upstream from IGS). M and S forms represent a model for the study of speciation at its early stage since they are diversifying in West and Central Africa despite some ongoing gene flow. In fact, M and S present some genome regions which are supposed to resist introgression – especially in the low-recombinant centromeric areas of chromosomes X and 2 (‘speciation islands’) – while the rest of the genome continuously homogenise. The observed pattern rises questions on whether divergence is essentially due to physical features of the genome that reduce recombination (e.g., centromeres) despite gene flow, or to selection on adaptive genes clustered in the centromeric ‘speciation islands’ or elsewhere in the genome. Hybrids between M and S are rare in nature, but an unusually high degree of hybridization was found at the western extreme of their distribution range (i.e.The Gambia and Guinea Bissau). This secondary contact zone represents an opportunity to investigate how reduced reproductive isolation affects genetic differentiation in genomic regions known to be segregated between M and S forms elsewhere in Africa. While most studies focus on high-throughput SNPs assays on limited sampling, we genotyped a large number of A. gambiae s.s. specimens from Guinea Bissau (and from other African countries for comparison) focusing on two intronic regions known to segregate in sympatric M and S molecular forms out from the hybridization area: i) the intron-4 of a cytochrome P450, namely the Cyp4G16 gene, which maps in the low recombination region of the X-centromere, ~7 kb upstream from SINE locus, and ii) the intron-1 of the voltage-gated sodium channel (VGSC) gene mapping on chromosome 2, out from the centromere area. Our results indicate that in the secondary contact zone recombination occurs within the most divergent region of M and S genome (i.e. the X-centromere), as highlighted by the intron-4 of Cyp4G16 data and support the hypothesis of asymmetric introgression from M to S, as shown by the analysis of intron-1 of VGSC gene.