Genomics of Population Divergence and Species Cohesion in an Ecologically Important Species Complex

Understanding the mechanisms underlying population divergence and species cohesion is central to population and conservation genomics, especially in taxa that function as foundation species for entire communities of animals and plants. In Eurasia, several phenotypically differentiated forms within the tree genus Populus have diverged in the face of gene flow. We explore the determinants of divergence and cohesion along this continuum, ranging from differentiated populations and phylogeographic lineages to divergent species with fairly strong postzygotic barriers (New Phytologist, 196:652-654, 2012; Molecular Ecology, 22:842-855, 2013; Molecular Ecology 23: 4316-4330, 2014). We report a whole genome sequencing (WGS) effort involving multiple populations of Eurasian Populus alba and P. tremula including multiple post-glacial recolonization lineages within the former. We find a complex genomic architecture of adaptive differentiation from both, standing genetic variation and new mutations. In Central European P. alba alone, screening of >1.7 million sequence polymorphisms reveals highly differentiated (≥4 std.dev.) outlier markers in >430 predicted genes. The genetic variation used by locally varying selection at the continent-wide scale appears to stem primarily from drift during glacial periods and admixture of colonizing lineages in interglacials. Genomic cohesion in hybridizing species appears to be maintained by widespread coupling effects (a.k.a. genome hitchhiking), although many of the studied genome windows (36% in Central Europe) do not exhibit any fixed between-species polymorphism. Cross-validation of pool-seq data with conventional genetic markers reveals the potentials and limits of WGS in the absence of a conspecific reference genome, which may inform related research programs in non-model taxa.