Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species

Abstract

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.

Patterns of genetic diversity and differentiation in resistance gene clusters of two hybridizing European Populus species

“…A strong decrease of F ST on the proximal end of chromosome XIX was found, confirming previous results by Macaya-Sanz et al (2011) and Stölting et al (2013). For this specific genome region, F ST values ranged from 0.000 to 0.216 and from 0.010 to 0.549 (Table S3) (Table S3).…”

“…In plants, resistance genes have been put forward for their potential role in the origin and maintenance of reproductive barriers through hybrid necrosis (Bomblies and Weigel 2007;Bomblies 2009). The two European Populus species, Populus alba and Populus tremula, have been described as species with incomplete reproductive barriers that hybridize despite relatively high levels of genomic divergence Lindtke et al 2012;Stölting et al 2013), largely concordant with available models of Bporous genomes^and heterogenous genomic divergence (Wu 2001;Feder et al 2012). Postzygotic selection has recently been put forward as a mechanism potentially maintaining the species barrier, but the exact selective factors acting on hybrid seedlings are currently unknown (Lindtke et al 2014).…”

“…European Populus species have previously been shown to present high levels of genomic divergence Lindtke et al 2012;Stölting et al 2013). The impact of R-gene clusters on the genomics of population divergence of Populus species with porous genomes is poorly known, even though R-genes were put forward as gene families that, through diversification by tandem duplication followed by genomic reorganization and gene conversion, have contributed greatly to the evolution of biological responses in poplars (Tuskan et al 2006).…”

“…Despite high overall genomic divergence in these species, it was shown that the proximal end of chromosome XIX presents a block of low interspecific divergence (Macaya-Sanz et al 2011;Stölting et al 2013). This genome region was proposed by Yin et al (2008) as an incipient sex chromosome, i.e., a chromosome morphologically similar to autosomes but in the process of developing characteristics of sex chromosomes.…”

Population genomics of the eastern cottonwood (Populus deltoides)

“…Several genomewide association, transcriptome, and population genomics studies have been reported for P. trichocarpa , contributing to the current knowledge about the species regulation of complex traits (McKown, Klápště, et al., 2014; Porth et al., 2013a, 2013b), extent of linkage disequilibrium (LD) and effective population size (Slavov et al., 2012; Zhou, Bawa, & Holliday, 2014), population structure (Geraldes et al., 2014; Slavov et al., 2012; Zhou et al., 2014), genetic diversity (Evans et al., 2014; Zhou et al., 2014), demographic history (Zhou et al., 2014), adaptation (Evans et al., 2014; Geraldes et al., 2014; Holliday, Zhou, Bawa, Zhang, & Oubida, 2016; Porth et al., 2015; Zhou et al., 2014), and sex determination (Geraldes et al., 2015). Studies in other poplar species (Stölting et al., 2013, 2015; Wang, Street, Scofield, & Ingvarsson, 2016a, 2016b) have significantly lagged behind. In fact, very limited population genetic information is available for widely distributed and ecologically and economically critical species such as Populus deltoides .…”