Reticulate speciation and adaptive introgression in theAnopheles gambiaespecies complex
Authors: Crawford Jacob E. , Riehle Michelle M. , Guelbeogo Wamdaogo M. , Gneme Awa , Sagnon N’Fale , Vernick Kenneth D. , Nielsen Rasmus , Lazzaro Brian P. 
Published: October 2014

Anopheles gambiae, the primary vector of human malaria in sub-Saharan Africa, exists as a series of ecologically specialized subgroups that are phylogenetically nested within theAnopheles gambiaespecies complex. These species and subgroups exhibit varying degrees of reproductive isolation, sometimes recognized as distinct subspecies. We have sequenced 32 complete genomes from field-captured individuals ofAnopheles gambiae,Anopheles gambiaeM form (recently namedA. coluzzii), sister speciesA. arabiensis, and the recently discovered “GOUNDRY” subgroup ofA.gambiaethat is highly susceptible toPlasmodium. Amidst a backdrop of strong reproductive isolation and adaptive differentiation, we find evidence for introgression of autosomal chromosomal regions among species and subgroups, some of which have facilitated adaptation. The X chromosome, however, is strongly differentiated among all species and subgroups, 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 amongA. gambiaeandA. arabiensisdespite strong divergence (∽5× higher than autosomal divergence) and isolation on the X chromosome. We find a large region of the X chromosome that has swept to fixation in the GOUNDRY subgroup within the last 100 years, which may be an inversion that serves as a partial barrier to contemporary gene flow. We show that speciation with gene flow results in genomic mosaicism of divergence and introgression. Such a reticulate gene pool connecting vector species and subgroups across the speciation continuum has 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 subgroups, although hybridization can facilitate sharing of globally adaptive alleles. Here, we show that differentiation and hybridization have acted in parallel in a species complex ofAnophelesmosquitoes 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 subgroups, 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 thatA. arabiensishas shared a mutation conferring insecticide resistance with two subgroups ofA. gambiaewithin 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.