Phylogenomics reveals a complex evolutionary history of lobed-leaf white oaks in western North America

Abstract

Species within the genus Quercus (oak) hybridize in complex patterns that have yet to be fully explored with phylogenomic data. Analyses to date have recovered reasonable divergent patterns, suggesting that the impact of introgression may not always be obvious in inferred oak phylogenies. We explore this phenomenon using RADseq data for 136 samples representing 54 oak species by conducting phylogenetic analyses designed to distinguish signals of lineage diversification and hybridization, focusing on the lobed-leaf species Quercus gambelii, Q. lobata, and Q. garryana in the context of a broad sampling of allied white oaks (Quercus section Quercus), and particularly the midwestern Q. macrocarpa. We demonstrate that historical introgressive hybridization between once sympatric species affects phylogeny estimation. Historical range expansion during periods of favorable climate likely explains our observations; analyses support genetic exchange between ancestral populations of Q. gambelii and Q. macrocarpa. We conclude that the genomic consequences of introgression caused the attraction of distant lineages in phylogenetic tree space, and that introgressive and divergent signals can be disentangled to produce a robust estimate of the phylogenetic history of the species.

Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity

“…The remaining five major clades are Quercus section Lobatae G.Don, the red oaks; Quercus section Protobalanus (Trelease) A.Camus, the intermediate or golden‐cup oaks; the sister species pair Quercus sadleriana R.Br. of California and Oregon, USA, and Q. pontica K.Koch of the western Caucasus Mountains and northern Turkey and Armenia (the Ponticae clade sensu McVay et al ., b); Quercus series Virentes Trel. [= Q. section Virentes Loudon]; and Quercus section Quercus , the white oaks, excluding Virentes and the Ponticae clade.…”

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

“…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 the past few years, restrictionsite‐associated DNA sequencing (RAD‐seq) and related methods (e.g., genotyping by sequencing, double‐digest RAD) have emerged as particularly efficient approaches to genotype as well as to identify SNPs for further study (Baird et al., 2008; Barchi et al., 2011; Davey & Blaxter, 2010; Pegadaraju, Nipper, Hulke, Qi, & Schultz, 2013; Scaglione et al., 2012). These methods have been applied with great success to understanding phylogeny, species circumscription, and hybridization patterns in oaks (Cavender‐Bares et al., 2015; Eaton, Hipp, González‐Rodríguez, & Cavender‐Bares, 2015; Fitz‐Gibbon, Hipp, Pham, Manos, & Sork, 2017; Hipp et al., 2014; McVay, Hauser, Hipp, & Manos, 2017). However, the costs are often relatively high per individual and require a library of identified individuals for comparison, making RAD‐seq and related methods impractical for identification of individual trees outside of the context of tree diversity research programs.…”

The Evolution of Tree Diversity: Proceedings of the 2016 IUFRO Genomics and Forest Tree Genetics Conference, Phylogenetics and Genomic Evolution Session, Arcachon, France

“…Hardin 1975) is lacking: phylogenetic informativeness of the plastome attenuates towards the tips of the white oaks, but it is not associated, at least in eastern North America, with strong phylogeographic signal. McVay et al (2017a) provide genomic evidence of historic introgression between a lobed white oak of eastern North America and two lobed white oaks of western North America that are no longer sympatric, resolving in the process an old phylogenetic puzzle: the placement of Quercus gambelii. The methods they use to tease apart the signal of ancient hybridization from that of population divergence in reduced-representation sequencing data augments the analytical toolkit for reconstructing the tree of life in hybridizing lineages.…”

“…Four papers in this volume use genomic approaches to investigate phylogenetic relationships in a genus or family. Two discussed above (McVay et al 2017a;Pham et al 2017) utilize the RAD-seq method to reconstruct phylogenetic relationships in the white oaks. RAD-seq, however, is still somewhat in its infancy for phylogenetics, and analytical approaches are not fully agreed upon (Ree and Hipp 2015).…”