Breakdown in the process of incipient speciation in Anopheles gambiae

Abstract

Understanding genetic causes and effects of speciation in sympatric populations of sexually reproducing eukaryotes ischallenging, controversial, and of practical importance for controlling rapidly evolving pests and pathogens. The major African malariavector mosquito Anopheles gambiae sensu stricto (s.s.) is considered to contain two incipient species with strong reproductiveisolation, hybrids between the M and S molecular forms being very rare. Following recent observations of higher proportions of hybridforms at a few sites in West Africa, we conducted new surveys of 12 sites in four contiguous countries (The Gambia, Senegal, Guinea-Bissau, and Republic of Guinea). Identification and genotyping of 3499 A. gambiae s.s. revealed high frequencies of M/S hybrid formsat each site, ranging from 5 to 42%, and a large spectrum of inbreeding coefficient values from 0.11 to 0.76, spanning most of therange expected between the alternative extremes of panmixia and assortative mating. Year-round sampling over 2 years at one of thesites in The Gambia showed that M/S hybrid forms had similar relative frequencies throughout periods of marked seasonal variation inmosquito breeding and abundance. Genome-wide scans with an Affymetrix high-density single-nucleotide polymorphism (SNP) microarrayenabled replicate comparisons of pools of different molecular forms, in three separate populations. These showed strongdifferentiation between M and S forms only in the pericentromeric region of the X chromosome that contains the molecular formspecificmarker locus, with only a few other loci showing minor differences. In the X chromosome, the M/S hybrid forms were moredifferentiated from M than from S forms, supporting a hypothesis of asymmetric introgression and backcrossing. © 2013 by the Genetics Society of America.