Title: Reticulate speciation and adaptive introgression in the Anopheles gambiae species

21 Anopheles gambiae, the primary vector of human malaria in sub-Saharan Africa, exists as 22 a series of ecologically specialized subgroups that are phylogenetically nested within the 23 Anopheles gambiae species complex. These species and subgroups exhibit varying 24 degrees of reproductive isolation, sometimes recognized as distinct subspecies. We have 25 sequenced 32 complete genomes from field-captured individuals of Anopheles gambiae, 26 Anopheles gambiae M form (recently named A. coluzzii), sister species A. arabiensis, and 27 the recently discovered “GOUNDRY” subgroup of A. gambiae that is highly susceptible 28 to Plasmodium. Amidst a backdrop of strong reproductive isolation and adaptive 29 differentiation, we find evidence for introgression of autosomal chromosomal regions 30 among species and subgroups, some of which have facilitated adaptation. The X 31 chromosome, however, is strongly differentiated among all species and subgroups, 32 pointing to a disproportionately large effect of X chromosome genes in driving speciation 33 among anophelines. Strikingly, we find that autosomal introgression has occurred from 34 contemporary hybridization among A. gambiae and A. arabiensis despite strong 35 divergence (~5× higher than autosomal divergence) and isolation on the X chromosome. 36 We find a large region of the X chromosome that has swept to fixation in the GOUNDRY 37 subgroup within the last 100 years, which may be an inversion that serves as a partial 38 barrier to contemporary gene flow. We show that speciation with gene flow results in 39 genomic mosaicism of divergence and introgression. Such a reticulate gene pool 40 connecting vector species and subgroups across the speciation continuum has important 41 implications for malaria control efforts. 42 43 Author Summary: 44 Subdivision of species into ecological specialized subgroups allows organisms to access a 45 wider variety of environments and sometimes leads to the formation of species 46 complexes. Adaptation to distinct environments tends to result in differentiation among 47 closely related subgroups, although hybridization can facilitate sharing of globally 48 adaptive alleles. Here, we show that differentiation and hybridization have acted in 49 parallel in a species complex of Anopheles mosquitoes that vector human malaria. In 50 particular, we show that extensive adaptive differentiation and partial reproductive 51 peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/009837 doi: bioRxiv preprint first posted online Oct. 1, 2014;