Taxonomic Relationships and Gene Flow in Four North American <I>Quercus</I> Species (<I>Quercus</I> section <I>Lobatae</I>)

Abstract

Taxonomic relationships between North American red oak species (Quercus section Lobatae) are not well resolved using genetic and morphological markers. Phenotypic plasticity, recent species divergence, and hybridization may all contribute to the unclear species boundaries in red oaks. We applied twenty-eight genomic and gene-based microsatellites, including outlier loci with potential roles in reproductive isolation and adaptive divergence between species, to natural populations of four monophyletic interfertile oak species: Quercus ellipsoidalis, Q. coccinea, Q. rubra, and Q. velutina. To better resolve the taxonomic relationships in this difficult clade, we assigned individual samples to species, identified hybrids and introgressive forms, and reconstructed phylogenetic relationships among the four species after exclusion of genetically intermediate individuals. Genetic assignment analyses identified four distinct species clusters, with Q. rubra most differentiated from the three other species. However, especially between Q. ellipsoidalis and Q. velutina, a comparatively large number of misclassified individuals (7.14%), hybrids (7.14%), and introgressive forms (18.83%) were detected. After the exclusion of genetically intermediate individuals, Q. ellipsoidalis grouped as sister species to the largely parapatric Q. coccinea with high bootstrap support (91%). Genetically intermediate forms in a mixed species stand were located proximate to both potential parental species, which supports recent hybridization of Q. velutina with both Q. ellipsoidalis and Q. rubra. Analyses of genome-wide patterns of interspecific differentiation can provide a better understanding of speciation processes and taxonomic relationships in this taxonomically difficult group of red oak species.

Adaptive Variation and Introgression of a CONSTANS-Like Gene in North American Red Oaks

“…ellipsoidalis/Q. coccinea clade [10]. This result is also supported by previous studies and a recent restriction site associated sequencing (RAD-seq) phylogeny of the genus ( [9,[11][12][13]).…”

“…This supports previous indications of recent and ongoing hybridization between Q. ellipsoidalis and Q. velutina [9,11]. Recent studies have shown gene flow between Q. rubra and the other three species to be more restricted, yet generally symmetric [9,10,15]. These four species also represent a drought tolerance gradient, with Q. rubra as the least drought tolerant followed by Q. velutina, Q. coccinea and lastly, Q. ellipsoidalis as the most drought tolerant [16,17].…”

“…DNA samples were obtained from 16 populations of four red oak species (Q. rubra, Q. ellipsoidalis, Q. velutina, and Q. coccinea) from the Great Lakes region (Wisconsin, Michigan, Illinois and Indiana; see Table S1 and Figure 1) [8,10,25]. The samples consisted of eight population pairs of Q. rubra and Q. ellipsoidalis (parapatric populations), six mixed stands of Q. ellipsoidalis and Q. velutina in proximity to unsampled Q. rubra populations (parapatric populations) and one mixed stand of Q. ellipsoidalis, Q. velutina, and Q. rubra (sympatric population).…”

“…This result is also supported by previous studies and a recent restriction site associated sequencing (RAD-seq) phylogeny of the genus ( [9,[11][12][13]). Genetically intermediate forms were found in contact zones between Q. ellipsoidalis, Q. rubra and Q. velutina, in sympatric stands indicating gene flow among these three species [8,10,14]. High levels of interspecific gene flow were detected especially between Q. ellipsoidalis and Q. velutina.…”

“…Hill-exhibit porous species boundaries and recent studies found strong evidence for contemporary interspecific gene flow in sympatric and parapatric stands based on genetic assignment and parentage analyses [5,[8][9][10]. Most recently, Owusu et al used both genic and nuclear microsatellite markers to better resolve the taxonomic relationships between these four species [10].…”