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.

Plant speciation across environmental gradients and the occurrence and nature of hybrid zones

“…Also evident is that highly diverged genomic regions detected by genomic scans represent a small component of the total genome and are often, though not always, spread across the genome rather than strongly clustered (Strasburg et al, ; Chapman et al, ; Brennan et al, ). Candidate genomic regions/genes affecting particular traits, possibly involved in adaptive divergence/reproductive isolation between species that form hybrid zones, have been identified by genomic scans (e.g., Christe et al, ), though have yet to be subjected to functional analysis.…”

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna

“…These include, in oaks, divergent selection (Ortego, Gugger, & Sork, 2017;Scotti-Saintagne et al, 2004), and asynchrony in flowering leading to assortative mating (Gailing & Curtu, 2014); in poplars, intrinsic incompatibility (Christe et al, 2017;Roe et al, 2014), and selection against hybrids (Christe et al, 2016). These include, in oaks, divergent selection (Ortego, Gugger, & Sork, 2017;Scotti-Saintagne et al, 2004), and asynchrony in flowering leading to assortative mating (Gailing & Curtu, 2014); in poplars, intrinsic incompatibility (Christe et al, 2017;Roe et al, 2014), and selection against hybrids (Christe et al, 2016).…”

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

“…Although not covered specifically in our study, WGS approaches are also certainly feasible in species groups originating from genome doubling, with available case studies spanning from recent autopolyploids to allopolyploids (products of past hybridization events; Zohren et al 2016) to paleopolyploids with ancient traces of whole-genome duplications (e.g. Christe et al 2017). This is good news for students of organismal groups in which genome doubling has evidently contributed to diversification, which includes many families of flowering plants (Soltis & Soltis 2016).…”

“…The successful integration of GBS and RAD-seq into studies of radiations was clearly facilitated by the development of user-friendly methods for de novo clustering of sequence reads (e.g. Catchen et al 2013) and by the availability of genome assemblies for reference-mapping and detecting DNA polymorphisms in model radiations often used by evolutionary biologists (The Heliconius Genome Consortium 2012; Brawand et al 2014;Christe et al 2017;Novikova et al 2016). There is considerable potential to extend this type of research to polyploids and taxa with variation in ploidy level, provided that appropriate statistical tools are used to detect and analyse genetic loci and allelic variation (e.g.…”

“…4B). In fact, a growing number of studies demonstrate that applying WGS to studies of speciation and radiation is entirely feasible, as long as an assembled and annotated reference genome and sufficient resources are available (The Heliconius Genome Consortium 2012; Brawand et al 2014;Ellegren 2014;Lamichhaney et al 2015;Christe et al 2017;McGee et al 2016;Novikova et al 2016). Although not covered specifically in our study, WGS approaches are also certainly feasible in species groups originating from genome doubling, with available case studies spanning from recent autopolyploids to allopolyploids (products of past hybridization events; Zohren et al 2016) to paleopolyploids with ancient traces of whole-genome duplications (e.g.…”