Article An Updated Infrageneric Classification of the North American Oaks (Quercus Subgenus Quercus): Review of the Contribution of Phylogenomic Data to Biogeography and Species Diversity Paul S. Manos 1,* and Andrew L. Hipp 2 1 Department of Biology, Duke University, 330 Bio Sci Bldg, Durham, NC 27708, USA 2 The Morton Arboretum, Center for Tree Science, 4100 Illinois 53, Lisle, IL 60532, USA; [email protected] * Correspondence: [email protected] Abstract: The oak flora of North America north of Mexico is both phylogenetically diverse and species-rich, including 92 species placed in five sections of subgenus Quercus, the oak clade centered on the Americas. Despite phylogenetic and taxonomic progress on the genus over the past 45 years, classification of species at the subsectional level remains unchanged since the early treatments by WL Trelease, AA Camus, and CH Muller. In recent work, we used a RAD-seq based phylogeny including 250 species sampled from throughout the Americas and Eurasia to reconstruct the timing and biogeography of the North American oak radiation. This work demonstrates that the North American oak flora comprises mostly regional species radiations with limited phylogenetic affinities to Mexican clades, and two sister group connections to Eurasia. Using this framework, we describe the regional patterns of oak diversity within North America and formally classify 62 species into nine major North American subsections within sections Lobatae (the red oaks) and Quercus (the Citation: Manos, P.S.; Hipp, A.L. An Quercus Updated Infrageneric Classification white oaks), the two largest sections of subgenus . We also distill emerging evolutionary and of the North American Oaks (Quercus biogeographic patterns based on the impact of phylogenomic data on the systematics of multiple Subgenus Quercus): Review of the species complexes and instances of hybridization. Contribution of Phylogenomic Data to Biogeography and Species Keywords: biodiversity; distribution; hybridization; oak; phylogeny; systematics Diversity. Forests 2021, 12, 786. https://doi.org/10.3390/f12060786 Academic Editors: Mary Ashley and 1. Introduction Janet R. Backs The oaks (Quercus, Fagaceae) comprise more than 435 species distributed across temperate and tropical regions of the northern hemisphere [1–3]. They are among the Received: 5 May 2021 best-known and most ecologically significant forest trees in North America (including Accepted: 10 June 2021 Mexico) and Eurasia, shaping forest and savanna ecosystems [4] and the diversity of urban Published: 15 June 2021 forests [5,6], and molding the development of human civilization and mythology [7–10]. Oaks are united by a suite of distinctive floral traits—in particular, pendant male catkins Publisher’s Note: MDPI stays neutral and tricarpellate female flowers with linear styles and expanded stigmas—and a signature with regard to jurisdictional claims in published maps and institutional affil- fruit trait: the circular single fruit or acorn seated within a cup-shaped extra-floral accessory iations. structure, a specialized involucre called a cupule. The cupule is the defining feature of Fagaceae. While other genera of the family feature acorns and valveless rounded cupules, the combination of floral character states shared by oaks is unique within the family [11,12]. The most recent classification system of Quercus recognizes eight sections within two subgenera, subgenus Quercus (ca. 295 spp.) and subg. Cerris (ca. 140 spp. [3]; Copyright: © 2021 by the authors. see Table1) . This old dichotomy between oak subgenera, which dates to the early Eocene, Licensee MDPI, Basel, Switzerland. was recognized in early molecular studies of the genus and family [13,14] and is robustly This article is an open access article distributed under the terms and supported by an extensive RAD-seq (next-generation DNA sequencing) phylogenomic conditions of the Creative Commons study of a comprehensive worldwide sample of species [15]. The two subgenera represent Attribution (CC BY) license (https:// a deep biogeographic split among modern taxa: subg. Cerris is restricted to Europe, Asia, creativecommons.org/licenses/by/ and northern Africa; and subg. Quercus, the American oak clade, is largely restricted to 4.0/). the Americas except for two dispersals back to Eurasia. Eight sections of the genus are Forests 2021, 12, 786. https://doi.org/10.3390/f12060786 https://www.mdpi.com/journal/forests Forests 2021, 12, 786 2 of 26 also supported by a combination of RAD-seq data and macro- and microscopic characters, most notably patterns of pollen ornamentation viewed under SEM [3]. These subtle yet well-established differences in pollen exine, and their correlation with phylogenomic data, give us high confidence in the basic split between subgenera and the pollen subtypes that correspond to each of the recognized sections [3,16]. Table 1. Current Infrageneric classification of the genus Quercus [3]. The total number of species with in each infrageneric group is provided, including the number of species within the Flora of North America (FNA) region and the number treated within this study. No. of Species No. of Species Quercus L. Sections Total/FNA Treated Here subg. Quercus 297/92 Lobatae Loud. 120/39 37 Protobalanus (Trel.) 5/5 Schwarz Ponticae Stef. 2/1 Virentes Loud. 7/4 Quercus 150/53 45 subg. Cerris Oerst. 138 Cyclobalanopsis (Oerst.) 90 Benth. & Hook. f. Cerris Dumort. 13 Ilex Loud. 35 Fossilized pollen has been used to pin the modern sections in time and space, serving as an invaluable resource to interpret paleobiogeography and to time-calibrate the global oak phylogeny [15,16]. Time-calibrated phylogenomic analyses, combined with fossil and modern oak species distributions, support an initial split in the American oak clade between the red oaks, sect. Lobatae, and the remainder of the clade between ca. 54 and 48 Ma (= million years ago). The non-Lobatae American oak clade sections exhibit high ecological diversity, with several striking contrasts between three early-diverging clades— sects. Protobalanus, Ponticae and Virentes—and the main radiation of white oaks, sect. Quercus. These early-branching lineages are species-poor, two to seven species each, restricted in distribution, and evergreen to wintergreen in habit. By contrast, sect. Quercus, with approximately 150 species of white oak, has the broadest distribution of all forest trees in the Northern Hemisphere [3]. This may be owing to the evolution of deciduousness and other traits associated with a range of continental climates, an exceptionally high range of functional diversity that sets the American oaks up as a model clade for understanding tree diversification and ecology [17,18]. The other main branch of the American oaks and the sister group to these lineages, sect. Lobatae, comprises the second largest clade next to the white oaks. It forms a remarkably parallel radiation to the white oaks with respect to distribution, habit, and morphology [17,19]. There is, however, an important point of ecological distinction between these two large oak clades: Lobatae show lower levels of diversification in western North America, especially in the California Floristic Province (CA-FP) and xeric woodlands of the American southwest [20]. The reasons for this ecological distinction between the clades may be key to understanding coexistence of these sections in the Americas, and the consequent interaction between diversification and tree diversity in oaks [17,21,22] The sectional classification for Quercus [3] is solid and unlikely to change. In this paper, we present a subsectional classification for the American oak clade based largely on our phylogenomic work of the past five years [15,19,23–25]. Our current sampling of Forests 2021, 12, 786 3 of 26 species for RAD-seq analysis stands at roughly 250 taxa: A total of 177 from subg. Quercus, the American oak clade, and 73 from subg. Cerris, the Eurasian oak clade. Within subg. Quercus, our coverage is nearly complete for the 92 species treated within the Flora of North America (FNA north of Mexico [1]). This phylogenomic work reveals compelling continental patterns of oak diversity at the broadest and narrowest phylogenetic scales. At the scale of entire clades, the early-branching clades as well as many other lineages within the two largest sections of subg. Quercus, sects. Lobatae (red oaks) and Quercus (white oaks), are distributed exclusively within North America north of Mexico (hereafter, “the FNA region”). It is also clear that the number of species within the FNA region with relationships to species outside the region is relatively low, limited to a single species of sect. Ponticae and a single clade in sect. Quercus, as discussed below. Thus, the oak flora of the FNA region is nearly a self-contained unit for study. At the same time, within regional clades, multiple radiations of taxa have been sampled at the population level for both our global phylogeny and as part of earlier stand-alone studies targeting the fine-scale systematics of challenging species complexes [23,25–28]. These enable the same dataset that informs classification to provide insight into species taxonomy. With this framework in place, we are well positioned to provide a phylogenetically-driven and timely bookend on the systematics of the taxa treated in the FNA region. Our goals with this review are: (1) To describe the biogeographic patterns of oak diversity within North America; (2) to formally classify 62 species into nine well-sampled monophyletic subsections; and (3) to review the impact of phylogenomic data on the systematics of multiple species complexes and distill the results of hypothesis testing involving hybridization within the flora. 1.1. Phylogeny and Biogeography of the Oak Flora in North America The American oak clade (Quercus subg. Quercus) comprises three endemic lineages— sects. Lobatae, Protobalanus and Virentes—and two Holarctic or transcontinental lineages— sects. Ponticae and Quercus (Figure1). Sections Lobatae, Protobalanus, and Quercus likely arose in what is now the boreal zone. Middle Eocene pollen records from Axel Heiberg Island (79◦55‘N, 88◦58‘ W) indicate the presence of modern oak lineages at high latitudes in North America by c.