Sex-Linked Differentiation Between Incipient Species of Anopheles gambiae

Abstract

Emerging species within the primary malaria vector Anopheles gambiae show different ecological preferences and significant prezygotic reproductive isolation. They are defined by fixed sequence differences in X-linked rDNA, but most previous studies have failed to detect large and significant differentiation between these taxa elsewhere in the genome, except at two other loci on the X chromosome near the rDNA locus. Hypothesizing that this pericentromeric region of the X chromosome may be accumulating differences faster than other regions of the genome, we explored the pattern and extent of differentiation between A. gambiae incipient species and a sibling species, A. arabiensis, from Burkina Faso, West Africa, at 17 microsatellite loci spanning the X chromosome. Interspecific differentiation was large and significant across the entire X chromosome. Among A. gambiae incipient species, we found some of the highest levels of differentiation recorded in a large region including eight independent loci near the centromere of the X chromosome. Outside of this region, no significant differentiation was detected. This pattern suggests that selection is playing a role in the emergence of A. gambiae incipient species. This process, associated with efficient exploitation of anthropogenic modifications to the environment, has public health implications as it fosters the spread of malaria transmission both spatially and temporally.

Ecological Zones Rather Than Molecular Forms Predict Genetic Differentiation in the Malaria VectorAnopheles gambiaes.s. in Ghana

“…gambiae may be separate entities that have been evolving under divergent selection pressures (Stump et al 2005), data from our study area suggest that interform gene flow is occurring at appreciable levels, perhaps most frequently in the southern mangrove strand zone of M/S sympatry. Our most striking and unexpected finding was of extremely strong genetic structure that correlated with ecological zones, with little, if any, contribution of distance, molecular form, and probably also chromosomal form.…”

“…The mean estimated null allele frequency of 8.7% was similar to the mean frequency of null alleles (5-8%) estimated for An. gambiae on the basis of X-linked loci in males (Barnes et al 2005;Stump et al 2005).…”

“…gambiae by della Torre et al (1997) and more recent evidence was provided by Turner et al (2005) who used a microarray approach to identify regions of the genome that they term ''islands of speciation.'' One of the regions that Turneret al (2005) identified does indeed appear to be intimately involved with the reproductive isolation of these forms (Stump et al 2005).…”

Centromere-proximal differentiation and speciation in Anopheles gambiae

“…Aside from sequences adjacent to the centromere of chromosome 2L and a small region of 2R (13,14), the most significant differentiation found to date has been at the centromeric end of the X chromosome (14,15). Nine microsatellite loci in an Ϸ5-megabase region of subdivisions 5B-6 have F ST values higher than any found elsewhere on the X or on other chromosomes (mean F ST ϭ 0.220, with values at a locus as high as 0.468) (15). In this same region, there is a nearly fixed difference in the insertion of a Maque transposable element at one locus, and strong frequency differences at others (16).…”

Molecular genetics: Bloodthirsty amazons?

“…Nonetheless, advances in molecular genetics are fast making Anopheles mosquitoes into valuable systems for studies of speciation and of both man-and climate-mediated evolution (Stump et al, 2005). Lisa Mirabello and Jan Conn discuss how mitochondrial sequence data suggest patterns of climate-induced change in the abundance of the Latin American malaria vector Anopheles darlingi (Mirabello and Conn, 2006).…”