A genetic legacy of introgression confounds phylogeny and biogeography in oaks

Abstract

Oaks (Quercus L.) have long been suspected to hybridize in nature, and widespread genetic exchange between morphologically defined species is well documented in two- to six-species systems, but the phylogenetic consequences of hybridization in oaks have never been demonstrated in a phylogenetically diverse sample. Here, we present phylogenomic analyses of a ca 30 Myr clade that strongly support morphologically defined species and the resolution of novel clades of white oaks; however, historical hybridization across clade boundaries is detectable and, undiagnosed, would obscure the imprint of biogeographic history in the phylogeny. Phylogenetic estimation from restriction-site-associated DNA sequencing data for 156 individuals representing 81 species supports two successive intercontinental disjunctions of white oaks: an early vicariance between the Eurasian and American white oaks, and a second, independent radiation represented by two relictual species. A suite of subsampled and partitioned analyses, however, supports a more recent divergence of the Eurasian white oaks from within the American white oaks and suggests that historic introgression between the Eurasian white oaks and a now-relictual lineage biases concatenated phylogenetic estimates. We demonstrate how divergence and reticulation both influence our understanding of the timing and nature of diversification and global colonization in these ecologically and economically important taxa.

Keywords: Quercus; RADseq; hybridization.

Figure 1.

Phylogeny and distribution. (a) Maximum-likelihood tree of the major clades of Quercus section Quercus (white oaks) rooted with species of section Protobalanus (grey). The early-branching position of the Roburoid clade (solid blue) is the result of concatenated analysis of the RAD data. The nested position of the Roburoid clade (dashed blue) is indicated by species tree estimation, and by targeted phylogenetic analyses conducted subsequent to detection of ancient hybridization between Q. pontica (yellow) and the Roburoid clade. White node represents New World derived (NWD) white oak clade. (b) Global distribution of Quercus section Quercus; black, NWD white oaks and series Virentes; blue, Roburoid clade; red, Q. sadleriana and yellow, Q. pontica of the Ponticae clade.

Figure 2.

Genomic evidence for introgressive hybridization across clade boundaries in white oaks. Comparison of the mean rank of relatedness of wild-collected individuals of Q. sadleriana (left) and Q. pontica (right). P-value represents expectation of observed rank of relatedness of Roburoid samples to the wild Q. pontica sample in the presence of incomplete lineage sorting. Observed rankings of Roburoids to Q. sadleriana sample did not differ significantly from simulated distribution. (Online version in colour.)

Figure 3.

Results of subsampling pseudoreplicate phylogenetic analyses. (a) Total evidence estimate; (b) exclusion of Ponticae samples; (c) dataset excluding Ponticae samples and loci that contain at least one Ponticae and one Roburoid; (d) reverse successive weighting—concatenated phylogenetic estimate of loci that do not favour monophyly of NWD white oaks; (e) reverse successive weighting—concatenated phylogenetic estimate of loci that do not favour monophyly of Ponticae. (Online version in colour.)