Rangewide population genetic structure of the African malaria vector Anopheles funestus

Abstract

Anopheles funestus is a primary vector of malaria in Africa south of the Sahara. We assessed its rangewide population genetic structure based on samples from 11 countries, using 10 physically mapped microsatellite loci, two per autosome arm and the X (N = 548), and 834 bp of the mitochondrial ND5 gene (N = 470). On the basis of microsatellite allele frequencies, we found three subdivisions: eastern (coastal Tanzania, Malawi, Mozambique and Madagascar), western (Burkina Faso, Mali, Nigeria and western Kenya), and central (Gabon, coastal Angola). A. funestus from the southwest of Uganda had affinities to all three subdivisions. Mitochondrial DNA (mtDNA) corroborated this structure, although mtDNA gene trees showed less resolution. The eastern subdivision had significantly lower diversity, similar to the pattern found in the codistributed malaria vector Anopheles gambiae. This suggests that both species have responded to common geographic and/or climatic constraints. The western division showed signatures of population expansion encompassing Kenya west of the Rift Valley through Burkina Faso and Mali. This pattern also bears similarity to A. gambiae, and may reflect a common response to expanding human populations following the development of agriculture. Due to the presumed recent population expansion, the correlation between genetic and geographic distance was weak. Mitochondrial DNA revealed further cryptic subdivision in A. funestus, not detected in the nuclear genome. Mozambique and Madagascar samples contained two mtDNA lineages, designated clade I and clade II, that were separated by two fixed differences and an average of 2% divergence, which implies that they have evolved independently for approximately 1 million years. Clade I was found in all 11 locations, whereas clade II was sampled only on Madagascar and Mozambique. We suggest that the latter clade may represent mtDNA capture by A. funestus, resulting from historical gene flow either among previously isolated and divergent populations or with a related species.

Restriction to gene flow is associated with changes in the molecular basis of pyrethroid resistance in the malaria vector Anopheles funestus

“…Previous work predicted that southern Africa was one interbreeding population based on continent-wide analysis (18), but genome-wide genetic diversity analysis using F st comparisons and Bayesian structure analysis has revealed three population clusters in southern Africa. Cluster 1, which includes Zambia and northern Malawi (SLM and NKK), corresponds to greater overexpression of CYP6M7.…”

Advances and Perspectives in the Study of the Malaria Mosquito Anopheles funestus

“…Temu et al [119], showed a similar pattern to the other studies at the country level for five countries in Eastern and Southern Africa: the genetic distance limited the gene flow among populations and promoted genetic differentiation among populations. A comprehensive study using samples across the continent provided important findings [93]. Anopheles funestus was subdivided into three large blocks: West Africa, East Africa and Central Africa [120,121].…”

“…funestus genome. They have allowed the analysis of population genetic structure, gene flow and demographic events across Africa [93], from Senegal [40], Cameroon [83,86], Kenya [94] to Madagascar [95], revealing important signatures of local adaptation, dispersion or speciation.…”

Inference of Population Structure Under a Dirichlet Process Model

“…The Bayesian method of Pritchard et al (2000) has the advantage that the uncertainty in the assignment of individuals to populations is easy to characterize. The method has also been of great practical importance, with uses in conservation genetics (Moodley and Harley 2005;Small et al 2006), epidemiology (Leo et al 2005;Michel et al 2005;Nejsum et al 2005;Ochsenreither et al 2006), and studies of population demography (e.g., Rosenberg et al 2002), and is often used as a first step in a genetic association study (Song and Elston 2006;Tsai et al 2006;Yu et al 2006).…”