Jacob Crawford, Michelle M. Riehle, Wamdaogo M. Guelbeogo, Awa Gneme, N’fale Sagnon, Kenneth D. Vernick, Rasmus Nielsen, Brian P. Lazzaro
Species complexes are common, especially among insect disease vectors, and understanding how barriers to gene flow among these populations become established or violated is critical for implementation of vector-targeting disease control. Anopheles gambiae, the primary vector of human malaria in sub-Saharan Africa, exists as a series of ecologically specialized populations that are phylogenetically nested within a species complex. These populations exhibit varying degrees of reproductive isolation, sometimes recognized as distinct subspecies. We have sequenced 32 complete genomes from field-captured individuals of Anopheles gambiae, Anopheles gambiae M form (recently named A. coluzzii), sister species A. arabiensis, and the recently discovered “GOUNDRY” subgroup of A. gambiae that is highly susceptible to Plasmodium. Amidst a backdrop of strong reproductive isolation and adaptive differentiation, we find evidence for adaptive introgression of autosomal chromosomal regions among species and populations. The X chromosome, however, remains strongly differentiated among all of the subpopulations, pointing to a disproportionately large effect of X chromosome genes in driving speciation among anophelines. Strikingly, we find that autosomal introgression has occurred from contemporary hybridization among A. gambiae and A. arabiensis despite strong divergence (~5× higher than autosomal divergence) and isolation on the X chromosome. We find a large region of the X chromosome that has recently swept to fixation in the GOUNDRY subpopulation, which may be an inversion that serves as a partial barrier to gene flow. We also find that the GOUNDRY population is highly inbred, implying increased philopatry in this population. Our results show that ecological speciation in this species complex results in genomic mosaicism of divergence and adaptive introgression that creates a reticulate gene pool connecting vector populations across the speciation continuum with important implications for malaria control efforts.