TY - JOUR T1 - Reticulate speciation and adaptive introgression in the <em>Anopheles gambiae</em> species complex JF - bioRxiv DO - 10.1101/009837 SP - 009837 AU - Jacob E. Crawford AU - Michelle M. Riehle AU - Wamdaogo M. Guelbeogo AU - Awa Gneme AU - N’fale Sagnon AU - Kenneth D. Vernick AU - Rasmus Nielsen AU - Brian P. Lazzaro Y1 - 2014/01/01 UR - http://biorxiv.org/content/early/2014/10/01/009837.abstract N2 - 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.Author Summary Subdivision of species into ecological specialized subgroups allows organisms to access a wider variety of environments and sometimes leads to the formation of species complexes. Adaptation to distinct environments tends to result in differentiation among closely related populations, although hybridization can facilitate sharing of globally adaptive alleles. Here, we show that differentiation and hybridization have acted in parallel in a species complex of Anopheles mosquitoes that vector human malaria. In particular, we show that extensive adaptive differentiation and partial reproductive isolation has led to genomic differentiation among mosquito species and populations, especially on the X chromosome. However, we also find evidence for exchange of genes on the autosomes that has provided the raw material for recent rapid adaptation. For example, we show that A. arabiensis has shared a mutation conferring insecticide resistance with two subgroups of A. gambiae within the last 60 years, illustrating the fluid nature of species boundaries among even more advanced species pairs. Our results underscore the expected challenges in deploying vector-based disease control strategies since many of the world’s most devastating human pathogens are transmitted by arthropod species complexes. ER -