Dissecting the genetic basis of differentiation and speciation in the Anopheles gambiae complex

AIM: The seven cryptic mosquito species of the Afrotropical Anopheles gambiae complex (Coluzzi et al., 2002, Science, 1415: 8) - and the M and S molecular forms within An. gambiae s.s. (della Torre, et al., 2005, IBMB, 755:69) - represents an emblematic example of fast adaptive radiation and incipient speciation, but the recent origin of this group creates relevant constraints to the reconstruction of its phylogenetic history. This speciation process strongly affects malaria epidemiology in sub-Saharan Africa, due to different ecology, behaviour and contribution to malaria transmission of the various species and forms. In fact, among them, some are major human malaria vectors, such as An. gambiae s.s. M and S forms, while others are minor or locally important vectors and non-vectors. Here are summarized the substantial progresses made in the understanding of the inter- and intra-specific diversification in this species-complex and some of the recent efforts to reconstruct their phylogenetic history. MATERIALS AND METHODS: Analyses on structural variations in polytene chromosomes (i.e. chromosomal paracentric inversions), estimation of genetic distances in sexual and autosomal loci and genotyping approaches through wide-genome scan (based on the An. gambiae reference genome; Holt et al., 2002, Science, 129: 49) were carried out in natural populations of the An. gambiae complex. Statistical analyses were performed to infer phylogenetic trees and to highlight population genetic structures. RESULTS: Data gathered so far on chromosomal inversions contributed to depict an evolutionary frame for the species complex (Ayala & Coluzzi, 2005, PNAS, Suppl. 1, 6535: 42; Sharakhov et al., in press), although it partially contradicts affinities expected on the basis of their ecology and adaptations. Moreover, chromosomal phylogeny is also not often consistent with reconstructions obtained with other molecular markers, due to shared ancestral polymorphisms and introgression events (reviewed in White et al., 2011, Annu. Rev. Ecol. Evol. Syst., 42: 111–132). Recent results also highlighted genomic areas and loci under positive selection that could be involved in the ongoing speciation process within An. gambiae s.s. (Lawniczak et al., 2010, Science, 512: 4) and that, thus, could have played instrumental roles in the ecotypic differentiation both within and across the semipermeable boundaries of M and S molecular forms. the genetic divergence within the An. gambiae complex, the reconstruction of a stable phylogeny among species and forms is still hindered by discrepancies between chromosomal and genetic data. Recent advances in genomic technologies will hopefully provide novel tools to resolve the conflicting results in the phylogeny of this group. A reliable reconstruction of the evolutionary history would allow to better understand the inheritance of evolutionary traits and adaptive abilities of these vector species, thereby helping in comprehending malaria epidemiology and optimizing effective vector- mediated control measures.