title: Selection against recombinant hybrids maintains reproductive isolation in hybridizing Populus species despite F1 fertility and recurrent gene flow.
abstract: Natural hybrid zones have proven to be precious tools for understanding the origin and maintenance of reproductive isolation (RI) and therefore species. Most available genomic studies of hybrid zones using whole- or partial-genome resequencing approaches have focused on comparisons of the parental source populations involved in genome admixture, rather than exploring fine-scale patterns of chromosomal ancestry across the full admixture gradient present between hybridizing species. We have studied three well-known European 'replicate' hybrid zones of Populus alba and P. tremula, two widespread, ecologically divergent forest trees, using up to 432 505 single-nucleotide polymorphisms (SNPs) from restriction site-associated DNA (RAD) sequencing. Estimates of fine-scale chromosomal ancestry, genomic divergence and differentiation across all 19 poplar chromosomes revealed strikingly contrasting results, including an unexpected preponderance of F1 hybrids in the centre of genomic clines on the one hand, and genomically localized, spatially variable shared variants consistent with ancient introgression between the parental species on the other. Genetic ancestry had a significant effect on survivorship of hybrid seedlings in a common garden trial, pointing to selection against early-generation recombinants. Our results indicate a role for selection against recombinant genotypes in maintaining RI in the face of apparent F1 fertility, consistent with the intragenomic 'coadaptation' model of barriers to introgression upon secondary contact. Whole-genome resequencing of hybridizing populations will clarify the roles of specific genetic pathways in RI between these model forest trees and may reveal which loci are affected most strongly by its cyclic breakdown.
authors.affiliation: Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700, Fribourg, Switzerland.
authors.forename: Camille
authors.initials: C
authors.lastname: Christe
authors.affiliation: Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700, Fribourg, Switzerland.
authors.forename: Kai N
authors.initials: KN
authors.lastname: Stölting
authors.affiliation: Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700, Fribourg, Switzerland.
authors.forename: Luisa
authors.initials: L
authors.lastname: Bresadola
authors.affiliation: Applied Forest Genetics, Bavarian Office for Forest Seeding and Planting, Forstamtsplatz 1, 83317, Teisendorf, Germany.
authors.forename: Barbara
authors.initials: B
authors.lastname: Fussi
authors.affiliation: Department of Genetics, Austrian Federal Research and Training Centre for Forests, Natural Hazards and Landscape, Seckendorff-Gudent-Weg 8, A-1130, Vienna, Austria.
authors.forename: Berthold
authors.initials: B
authors.lastname: Heinze
authors.affiliation: Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700, Fribourg, Switzerland.
authors.forename: Daniel
authors.identifier: 0000-0003-2866-6739
authors.initials: D
authors.lastname: Wegmann
authors.affiliation: Department of Biology, University of Fribourg, Chemin du Musée 10, CH-1700, Fribourg, Switzerland.|Department of Botany and Biodiversity Research, University of Vienna, Rennweg 14, A-1030, Vienna, Austria.
authors.forename: Christian
authors.initials: C
authors.lastname: Lexer
mesh_terms: D018742:DNA, Chloroplast / Q000235:genetics; D018744:DNA, Plant / Q000235:genetics; D005298:Fertility; D051456:Gene Flow; D005828:Genetics, Population; D018745:Genome, Plant; D005838:Genotype; D006239:Haplotypes; D006824:Hybridization, Genetic; D015810:Linkage Disequilibrium; D020641:Polymorphism, Single Nucleotide; D032107:Populus / Q000235:genetics*; D060047:Reproductive Isolation; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA
chemical_list: D018742:DNA, Chloroplast; D018744:DNA, Plant
keywords: Hybrid zones; Populus; RAD; admixture; common garden; differentiation; divergence; genotyping by sequencing; local genetic ancestry; speciation