Genomic Identity of White Oak Species in an Eastern North American Syngameon

Andrew L. Hipp, Alan T. Whittemore, Mira Garner, Marlene Hahn, Elisabeth Fitzek, Erwan Guichoux, Jeannine Cavender-Bares, Paul F. Gugger, Paul S. Manos, Ian S. Pearse, Charles H. Cannon

Research output: Contribution to journalArticlepeer-review

5 Scopus citations

Abstract

The eastern North American white oaks, a complex of approximately 16 potentially interbreeding species, have become a classic model for studying the genetic nature of species in a syngameon. Genetic work over the past two decades has demonstrated the reality of oak species, but gene flow between sympatric oaks raises the question of whether there are conserved regions of the genome that define oak species. Does gene flow homogenize the entire genome? Do the regions of the genome that distinguish a species in one part of its range differ from the regions that distinguish it in other parts of its range, where it grows in sympatry with different species? Or are there regions of the genome that are relatively conserved across species ranges? In this study, we revisit seven species of the eastern North American white oak syngameon using a set of 80 single-nucleotide polymorphisms (SNPs) selected in a previous study because they show differences among, and consistency within, the species. We test the hypothesis that there exist segments of the genome that do not become homogenized by repeated introgression, but retain distinct alleles characteristic of each species. We undertake a range-wide sampling to investigate whether SNPs that appeared to be fixed based on a relatively small sample in our previous work are fixed or nearly fixed across the range of the species. Each of the seven species remains genetically distinct across its range, given our diagnostic set of markers, with relatively few individuals exhibiting admixture of multiple species. SNPs map back to all 12 Quercus linkage groups (chromosomes) and are separated from each other by an average of 7.47 million bp (± 8.74 million bp, SD), but are significantly clustered relative to a random null distribution, suggesting that our SNP toolkit reflects genome-wide patterns of divergence while potentially being concentrated in regions of the genome that reflect a higher-than-average history of among-species divergence. This application of a DNA toolkit designed for the simple problem of identifying species in the field has two important implications. First, the eastern North American white oak syngameon is composed of entities that most taxonomists would consider "good species." Second, and more fundamentally, species in the syngameon are genetically coherent because characteristic portions of the genome remain divergent despite a history of introgression. Understanding the conditions under which some loci diverge while others introgress is key to understanding the origins and maintenance of global tree diversity.

Original languageEnglish (US)
Pages (from-to)455-477
Number of pages23
JournalAnnals of the Missouri Botanical Garden
Volume104
Issue number3
DOIs
StatePublished - Oct 1 2019

Bibliographical note

Funding Information:
1 This paper is based on a talk presented by the first author at the Missouri Botanical Garden’s 65th Annual Fall Symposium. Portions of the introduction and conclusion are adapted from an essay published by the first author in the Journal of International Oaks (Hipp, 2015). The manuscript benefited from comments by Thibault Leroy. Data and analyses presented here have not been published elsewhere. The majority of collections and all of M. G.’s time were funded by USDA Agreement Number 58-8020-5-005, project number 8020-21000-070-03S, to A. L. H. and A. T. W. Leaf silhouettes were digitized in part by M. Kaproth. SNP data were generated with financial support of The Morton Arboretum’s Center for Tree Science. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government. 2 The Morton Arboretum, Herbarium, 4100 Illinois Route 53, Lisle, Illinois 60532, U.S.A. 3 Integrative Research Center, The Field Museum, 1400 S Lake Shore Drive, Chicago, Illinois 60605, U.S.A. 4 U.S. National Arboretum, 3501 New York Avenue NE, Washington, D.C. 20002, U.S.A. 5 Universität Bielefeld, Department of Computational Biology, Center for Biotechnology - CeBiTec, Universitaetsstrasse 27, 33615 Bielefeld, Germany. 6 BIOGECO, INRA, Université Bordeaux, 33610 Cestas, France. 7 Department of Ecology, Evolution and Behavior, University of Minnesota, 1479 Gortner Avenue, Saint Paul, Minnesota 55108, U.S.A. 8 University of Maryland Center for Environmental Science, Appalachian Laboratory, 301 Braddock Road, Frostburg, Maryland 21532, U.S.A. 9 Department of Biology, Duke University, 130 Science Drive, Durham, North Carolina 27708, U.S.A. 10 U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Fort Collins, Colorado 80526, U.S.A. * Author for correspondence: ahipp@mortonarb.org

Keywords

  • Cohesion species
  • DNA genotyping toolkit
  • Quercus
  • hybridization
  • introgression
  • single-nucleotide polymorphism (SNP)
  • syngameon

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