Speciation as a process remains a central focus of evolutionary biology, but our
understanding of the genomic architecture and prevalence of speciation in the face of gene
flow remains incomplete. The Anopheles gambiae species complex of malaria
mosquitoes is a radiation of ecologically diverse taxa. This complex is well-suited for
testing for evidence of a speciation continuum and genomic barriers to introgression
because its members exhibit partially overlapping geographic distributions as well as
varying levels of divergence and reproductive isolation. We sequenced 20 genomes from wild
A. gambiae s.s., Anopheles coluzzii, Anopheles
arabiensis, and compared these with 12 genomes from the “GOUNDRY” subgroup of
A. gambiae s.l. Amidst a backdrop of strong
reproductive isolation, we find strong evidence for a speciation continuum with
introgression of autosomal chromosomal regions among species and subgroups. The X
chromosome, however, is strongly differentiated among all taxa, 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 between A. gambiae and A.
arabiensis despite strong divergence (∼5× higher than autosomal divergence) and
isolation on the X chromosome. In addition to the X, we find strong evidence that lowly
recombining autosomal regions, especially pericentromeric regions, serve as barriers to
introgression secondarily to the X. We show that speciation with gene flow results in
genomic mosaicism of divergence and introgression. Such a reticulate gene pool connecting
vector taxa across the speciation continuum has important implications for malaria control
efforts.