Genomic divergence and introgression among three Populus species

Genomic divergence with gene flow is very common in both plants and animals. However, divergence and gene flow are two counteracting factors during speciation. Identifying the types of genes that are likely to be introgressed and what genetic factors restrict further effective reproduction of interspecific hybrids is of great interest to biologists. We aimed to address these issues using three related tree species, Populus alba (Pa), P. tremula (Pt), and P. tremuloides (Ps), and the interspecific hybrid of the former two species, P. × canescens (Pc). We collected 105 genomes for these four poplar lineages, including 28 Pa, 38Pt, 21 Ps, and 18 Pc individuals, to reconstruct their evolutionary histories. Our coalescence-based simulations indicated that Pa diverged earliest from Ps and Pt, and asymmetrical gene flow existed between any two lineages, with especially large ancient gene flow occurring between Pa and Pt. The genomic landscape of divergence between pairs of the three species are highly heterogeneous, which may have arisen through both divergent sorting of ancient polymorphisms and ongoing gene flow. We found that extant regions of the genome with introgressed ancestry reduced genetic divergence but elevated recombination rates and accounted for 5.76 % of the total genome. Introgressed genes were functionally associated with stress resistance, including innate immune response, anti-adversity response, and programmed cell death. However, candidate genes underlying postmating barriers of Pc were homozygous and resistant to introgression due to the incompatibility of alleles between loci after hybridization and were associated with endosperm and gamete formation and disease resistance. Our study revealed genomic dynamics during speciation with gene flow and identified regions of the genome that were likely introgressed and adaptive as well as candidate loci responsible for hybrid incompatibility that resulted in the formation of postmating barriers after hybridization.