Abstract
Anopheles gambiae s.l. are important malaria vectors, but little is known about their genomic variation in the wild. Here, we present inter- and intraspecies analysis of genome-wide RADseq data, in three Anopheles gambiae s.l. species collected from East Africa. The mosquitoes fall into three genotypic clusters representing described species (A. gambiae, A. arabiensis, and A. merus) with no evidence of cryptic breeding units. Anopheles merus is the most divergent of the three species, supporting a recent new phylogeny based on chromosomal inversions. Even though the species clusters are well separated, there is extensive shared polymorphism, particularly between A. gambiae and A. arabiensis. Divergence between A. gambiae and A. arabiensis does not vary across the autosomes but is higher in X-linked inversions than elsewhere on X or on the autosomes, consistent with the suggestion that this inversion (or a gene within it) is important in reproductive isolation between the species. The 2La/2L+a inversion shows no more evidence of introgression between A. gambiae and A. arabiensis than the rest of the autosomes. Population differentiation within A. gambiae and A. arabiensis is weak over approximately 190–270 km, implying no strong barriers to dispersal. Analysis of Tajima’s D and the allele frequency spectrum is consistent with modest population increases in A. arabiensis and A. merus, but a more complex demographic history of expansion followed by contraction in A. gambiae. Although they are less than 200 km apart, the two A. gambiae populations show evidence of different demographic histories.
Highlights
In their role as vectors of malaria, Anopheles mosquitoes were indirectly responsible for an estimated 600,000 deaths in sub-Saharan Africa in 2010 (World Health Organization 2012)
This is partly due to divergence of A. arabiensis and A. merus from the PEST genome and due to polymorphisms in the genomes at the restriction sites; the more samples and species that are included, the more likely a RAD tag will be absent in one or more samples
The proportion of reads aligning to exons was about twice as high for the X chromosome as for the autosomes (27% vs. 13%, 40% vs. 17%, and 43% vs. 19% for A. gambiae, A. arabiensis, and A. merus, respectively)
Summary
In their role as vectors of malaria, Anopheles mosquitoes were indirectly responsible for an estimated 600,000 deaths in sub-Saharan Africa in 2010 (World Health Organization 2012). Knowledge of the genetics of wild populations of these mosquitoes is important for both conventional and novel vector control methods. Conventional control of vectors by insecticide-treated bed nets and indoor residual spraying can be hampered by the spread of insecticide resistance (Enayati and Hemingway 2010), and in the case of novel control methods such as sterile insect technique (SIT) and introduction of transgenes, a knowledge of the size of mosquito populations (which can be estimated indirectly by genetic diversity) and population structure will be required (James 2005). Within A. gambiae s.l., the most important vectors are the widespread species A. gambiae and A. arabiensis, all other members of the complex are malaria vectors, with the exception of A. quadriannulatus and A. amharicus (formerly A. quadriannulatus B, Coetzee et al 2013). All species within the complex will produce fertile female offspring in laboratory crosses (Davidson 1964), but with the exception of A. gambiae  A. coluzzii (formerly A. gambiae S and M form, Coetzee et al 2013); male offspring are infertile
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