A genetic legacy of introgression confounds phylogeny and biogeography in oaks

Abstract

Oaks ( 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 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.

A nuclear DNA barcode for eastern North American oaks and application to a study of hybridization in an Arboretum setting

“…The matrix of 119 SNPs was chosen for design of two final multiplexes to ensure a selection of 80 SNPs via the primer design suite across two multiplexes. Maximum‐likelihood (ML) phylogenetic analysis was then conducted for each matrix to evaluate whether each SNP set could identify species known from prior work (Hipp et al., 2018; McVay, Hipp et al., 2017) to be monophyletic. Phylogenetic analysis was conducted using PhyML (Guindon et al., 2010) with mode = “A la carte” and number of bootstraps = 100, as implemented in phylogeny.fr (Dereeper et al., 2008).…”

“…For marker development, we used RAD‐seq data from 63 samples selected to represent 15 species or species groups (Supplementary File 1) reported from a previous study (McVay, Hipp et al., 2017). Quercus muehlenbergii and Q. prinoides were treated together as a single species in our study, because our analyses as well as current phylogenetic work (McVay, Hipp et al., 2017; Pham, Hipp, Manos, & Cronn, 2017) suggest that the two are not distinguishable using multilocus nuclear data.…”

“…Quercus muehlenbergii and Q. prinoides were treated together as a single species in our study, because our analyses as well as current phylogenetic work (McVay, Hipp et al., 2017; Pham, Hipp, Manos, & Cronn, 2017) suggest that the two are not distinguishable using multilocus nuclear data. The European white oaks and East Asian white oaks were treated as two species groups to identify markers that distinguish the two groups from one another and to study possible patterns of gene flow between American and Eurasian white oak.…”

“…RAD‐seq DNA extraction, library preparation, and sequencing were conducted as presented previously in oaks (Cavender‐Bares et al., 2015; Hipp et al., 2014, 2018; McVay, Hauser et al., 2017, McVay, Hipp et al., 2017). Briefly, DNA for all RAD‐seq samples was extracted from fresh or frozen material using the DNeasy plant extraction protocol (DNeasy, Qiagen, Valencia, CA, USA).…”

“…In this study, we present an 80‐SNP DNA barcode for species identification and hybrid studies of a suite of common eastern North American white oaks. Our addresses solves the problem of identifying barcode‐informative loci through careful selection of a core set of informative and easily amplified SNPs from a broadly sampled RAD‐seq dataset (McVay, Hipp, & Manos, 2017). We then develop PCR primers for multiplex amplification and SNP genotyping using the MassARRAY platform and apply this DNA barcode to a pilot study of hybridization among white oaks in the living collections of The Morton Arboretum.…”