Interspecific genetic exchange structures genomic constitution, where past and ongoing introgression has resulted in mosaic genomes. Such genomic heterogeneity ultimately reflects the role of selection in constraining or facilitating gene exchange across taxa. Loci under divergent [or balancing] selection are impermeable [or maintained] in the face of introgression, which results in higher [or lower] differentiation compared to the neutral background that reflects average genome-wide interspecific gene exchange. The genic species concept along with hitchhiking effects predicts that the progression of speciation can be tracked as it should generate predictable patterns such as the increase of genome impermeability as speciation advances. A steady increase in the number of impermeable loci along with a corresponding decrease in permeable loci should reflect accumulating impermeability as speciation progresses. Here we used restriction site-associated DNA sequencing (RADSeq) to conduct a genomic survey on an alder (Alnus) species complex with a history of secondary contact during the postglacial period across Alaska and Yukon. We used a combination of FST-outlier analysis, geographic clines, and genomic clines to bin SNP loci into one of the three categories (impermeable, permeable, or maintained) and computed the ratios across loci type.
Results/Conclusions
Our results provide a direct test of the genic species concept. The proportions across the three types of loci varied as predicted along the speciation continuum. Genomic patterns of introgression revealed 2%, 84%, and 14% impermeable, permeable, and maintained loci, respectively, between two glacial lineages of the same subspecies (Alnus viridis subsp. fruticosa). The proportions were 6%, 64%, and 30% between two subspecies of the same species (A. v. subsp. fruticosa and A. v. susp. sinuata), and 56%, 30%, and 14% between two species (A. v. subsp. fruticosa and A. incana subsp. tenuifolia). The differences are all statistically significant between these taxa. Thus the number of impermeable loci increases while the number of permeable loci decreases along the speciation continuum. These results support the genic species concept suggesting that genes are the primary unit of species differentiation and that speciation should have tractable patterns at the level of genes. This study represents a first step for elucidating key patterns of speciation, and as similar analyses are calculated across other systems, it will be possible to quantify the ranges of permeability across the speciation continuum.