Genomic Identity of White Oak Species in an Eastern North American Syngameon1

• Published in: Annals of the Missouri Botanical Garden 2019-09, Vol.104 (3), p.455-477
• Main Authors: Hipp, Andrew L, Whittemore, Alan T, Garner, Mira, Hahn, Marlene, Fitzek, Elisabeth, Guichoux, Erwan, Cavender-Bares, Jeannine, Gugger, Paul F, Manos, Paul S, Pearse, Ian S, Cannon, Charles H
• Format: Article
• Language: English
• Subjects: Cohesion species; DNA genotyping toolkit; hybridization; introgression; Quercus; single-nucleotide polymorphism (SNP); syngameon
• ISSN: 0026-6493; 2162-4372
• DOI: 10.3417/2019434

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 d