Admixture between genetically divergent populations facilitates genomic studies of the mechanisms involved in adaptation, reproductive isolation, and speciation, including mapping of the loci involved in these phenomena. Little is known about how pre-and postzygotic barriers will affect the prospects of ''admixture mapping'' in wild species. We have studied 93 mapped genetic markers (microsatellites, indels, and sequence polymorphisms, $60,000 data points) to address this topic in hybrid zones of Populus alba and P. tremula, two widespread, ecologically important forest trees. Using genotype and linkage information and recently developed analytical tools we show that (1) reproductive isolation between these species is much stronger than previously assumed but this cannot prevent the introgression of neutral or advantageous alleles, (2) unexpected genotypic gaps exist between recombinant hybrids and their parental taxa, (3) these conspicuous genotypic patterns are due to assortative mating and strong postzygotic barriers, rather than recent population history. We discuss possible evolutionary trajectories of hybrid lineages between these species and outline strategies for admixture mapping in hybrid zones between highly divergent populations. Datasets such as this one are still rare in studies of natural hybrid zones but should soon become more common as high throughput genotyping and resequencing become feasible in nonmodel species.

Recent advances in population genomics have triggered great interest in the genomic landscape of divergence in taxa with ‘porous’ species boundaries. One important obstable of previous studies of this topic was the low genomic coverage achieved. This issue can now be overcome by the use of ‘next generation’ or short‐read DNA‐sequencing approaches capable of assaying many thousands of single nucleotide polymorphisms (SNPs) in divergent species. We have scanned the ‘porous’ genomes of Populus alba and Populus tremula, two ecologically divergent hybridizing forest trees, using >38 000 SNPs assayed by restriction site associated DNA (RAD) sequencing. Windowed analyses indicate great variation in genetic divergence (e.g. the proportion of fixed SNPs) between species, and these results are unlikely to be strongly biased by genomic features of the Populus trichocarpa reference genome used for SNP calling. Divergence estimates were significantly autocorrelated (P < 0.01; Moran's I up to 0.6) along 11 of 19 chromosomes. Many of these autocorrelations involved low divergence blocks, thus suggesting that allele sharing was caused by recurrent gene flow rather than shared ancestral polymorphism. A conspicuous low divergence block of three megabases was detected on chromosome XIX, recently put forward as an incipient sex chromosome in Populus, and was largely congruent with introgression of mapped microsatellites in two natural hybrid zones (N > 400). Our results help explain the origin of the ‘genomic mosaic’ seen in these taxa with ‘porous’ genomes and suggest rampant introgression or extensive among‐species conservation of an incipient plant sex chromosome. RAD sequencing holds great promise for detecting patterns of divergence and gene flow in highly divergent hybridizing species.

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The maintenance of species barriers in the face of gene flow is often thought to result from strong selection against intermediate genotypes, thereby preserving genetic differentiation. Most speciation genomic studies thus aim to identify exceptionally divergent loci between populations, but divergence will be affected by many processes other than reproductive isolation (RI) and speciation. Through genomic studies of recombinant hybrids sampled in the wild, genetic variation associated with RI can be observed in situ, because selection against incompatible genotypes will leave detectable patterns of variation in the hybrid genomes. To better understand the mechanisms directly involved in RI, we investigated three natural 'replicate' hybrid zones between two divergent Populus species via locus-specific patterns of ancestry across recombinant hybrid genomes. As expected, genomic patterns in hybrids and their parental species were consistent with the presence of underdominant selection at several genomic regions. Surprisingly, many loci displayed greatly increased between-species heterozygosity in recombinant hybrids despite striking genetic differentiation between the parental genomes, the opposite of what would be expected with selection against intermediate genotypes. Only a limited, reproducible set of genotypic combinations was present in hybrid genomes across localities. In the absence of clearly delimited 'hybrid habitats', our results suggest that complex epistatic interactions within genomes play an important role in advanced stages of RI between these ecologically divergent forest trees. This calls for more genomic studies that test for unusual patterns of genomic ancestry in hybridizing species.

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