Reticulate Speciation and Barriers to Introgression in theAnopheles gambiaeSpecies Complex

Abstract

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.

Fine-scale species delimitation: speciation in process and periodic patterns in nudibranch diversity

“…There is a possible window for crossbreeding and subsequent gene flow during periods of storms or upwelling when the surface layer above the halocline temporarily attains a higher salinity, rendering it available for A. andra sp. nov. Any species, while forming, must pass through this "reticulated phase" of genetic exchange (e.g., Hennig 1966;Crawford et al 2015) when it still retains some partial connection with its ancestral species; thus, this case is not only of particular taxonomic interest, but of general evolutionary importance. Recently, multiple evidence was obtained for a very recent speciation event when closely related species formed a reticulated pattern (Burress et al 2018).…”

Living Organisms Author Their Read-Write Genomes in Evolution

“…The importance of introgressive hybridization between distinct populations in their evolutionary development is yet another factor that has led certain authors to point out that it is more appropriate to consider reticulate (net-like) over conventional branching (tree-like) models for inheritance by new species [ 158 , 159 , 160 ]. Altogether, we can see from the Geospiza , cichlid, and other cases like those cited in Table 4 , that biological activity in the form of interspecific hybridization provides a key impetus to many (perhaps most?)…”

Chromosomal Speciation in the Genomics Era: Disentangling Phylogenetic Evolution of Rock-wallabies

“…At the same time, evidence from genome comparisons is revealing that reticulate evolution, including introgression across distantly related species, is far more common in animals than previously thought ( Mallet et al, 2016 ) with implications for gene-tree – species-tree discordance ( Edwards et al, 2016 ). This directs attention to the potential for differing extents of introgression within and outside rearranged regions of the genome ( Noor and Bennett, 2009 ; Crawford et al, 2015 ).…”