title: Adaptive evolution and segregating load contribute to the genomic landscape of divergence in two tree species connected by episodic gene flow.
abstract: Speciation often involves repeated episodes of genetic contact between divergent populations before reproductive isolation (RI) is complete. Whole-genome sequencing (WGS) holds great promise for unravelling the genomic bases of speciation. We have studied two ecologically divergent, hybridizing species of the 'model tree' genus Populus (poplars, aspens, cottonwoods), Populus alba and P. tremula, using >8.6 million single nucleotide polymorphisms (SNPs) from WGS of population pools. We used the genomic data to (i) scan these species' genomes for regions of elevated and reduced divergence, (ii) assess key aspects of their joint demographic history based on genomewide site frequency spectra (SFS) and (iii) infer the potential roles of adaptive and deleterious coding mutations in shaping the genomic landscape of divergence. We identified numerous small, unevenly distributed genome regions without fixed polymorphisms despite high overall genomic differentiation. The joint SFS was best explained by ancient and repeated gene flow and allowed pinpointing candidate interspecific migrant tracts. The direction of selection (DoS) differed between genes in putative migrant tracts and the remainder of the genome, thus indicating the potential roles of adaptive divergence and segregating deleterious mutations on the evolution and breakdown of RI. Genes affected by positive selection during divergence were enriched for several functionally interesting groups, including well-known candidate 'speciation genes' involved in plant innate immunity. Our results suggest that adaptive divergence affects RI in these hybridizing species mainly through intrinsic and demographic processes. Integrating genomic with molecular data holds great promise for revealing the effects of particular genetic pathways on speciation.
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: Margot
authors.initials: M
authors.lastname: Paris
authors.affiliation: Institut des Sciences de l'Evolution (UMR 5554), CNRS-UM2-IRD, Place Eugene Bataillon, F-34095, Montpellier, France.|Station Méditerranéenne de l'Environnement Littoral, Université Montpellier 2, 2 Rue des Chantiers, F-34200, Séte, France.
authors.forename: Christelle
authors.initials: C
authors.lastname: Fraїsse
authors.affiliation: Institut des Sciences de l'Evolution (UMR 5554), CNRS-UM2-IRD, Place Eugene Bataillon, F-34095, Montpellier, France.|Station Méditerranéenne de l'Environnement Littoral, Université Montpellier 2, 2 Rue des Chantiers, F-34200, Séte, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Bierne
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: D019143:Evolution, Molecular; D051456:Gene Flow; D018745:Genome, Plant; D023281:Genomics; D020641:Polymorphism, Single Nucleotide; D032107:Populus / Q000145:classification / Q000235:genetics*; D060047:Reproductive Isolation; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D014197:Trees / Q000145:classification / Q000235:genetics
keywords: 
  Populus
  ; divergence; pool-seq; secondary contact; selection; speciation