Plastome data reveal multiple geographic origins ofQuercusGroup Ilex

Abstract

Nucleotide sequences from the plastome are currently the main source for assessing taxonomic and phylogenetic relationships in flowering plants and their historical biogeography at all hierarchical levels. One major exception is the large and economically important genus Quercus (oaks). Whereas differentiation patterns of the nuclear genome are in agreement with morphology and the fossil record, diversity patterns in the plastome are at odds with established taxonomic and phylogenetic relationships. However, the extent and evolutionary implications of this incongruence has yet to be fully uncovered. The DNA sequence divergence of four Euro-Mediterranean Group Ilex oak species (Quercus ilex L., Q. coccifera L., Q. aucheri Jaub. & Spach., Q. alnifolia Poech.) was explored at three chloroplast markers (rbcL, trnK/matK, trnH-psbA). Phylogenetic relationships were reconstructed including worldwide members of additional 55 species representing all Quercus subgeneric groups. Family and order sequence data were harvested from gene banks to better frame the observed divergence in larger taxonomic contexts. We found a strong geographic sorting in the focal group and the genus in general that is entirely decoupled from species boundaries. High plastid divergence in members of Quercus Group Ilex, including haplotypes shared with related, but long isolated oak lineages, point towards multiple geographic origins of this group of oaks. The results suggest that incomplete lineage sorting and repeated phases of asymmetrical introgression among ancestral lineages of Group Ilex and two other main Groups of Eurasian oaks (Cyclobalanopsis and Cerris) caused this complex pattern. Comparison with the current phylogenetic synthesis also suggests an initial high- versus mid-latitude biogeographic split within Quercus. High plastome plasticity of Group Ilex reflects geographic area disruptions, possibly linked with high tectonic activity of past and modern distribution ranges, that did not leave imprints in the nuclear genome of modern species and infrageneric lineages.

Development of Chloroplast and Nuclear DNA Markers for Chinese Oaks (Quercus Subgenus Quercus) and Assessment of Their Utility as DNA Barcodes

“…Within Group Ilex , species of the morphological Sections Heterbalanus, Engleriana, and Echinolepides are mixed and form multiple clades without clear boundaries in the NJ trees (i.e., Figures 3 and Figure S13), albeit the oaks among the three morphology-based sections show distinct morphological differences in foliage and acorn cupule patterns (Pu et al, 2002; Peng et al, 2007). Previous phylogenetic studies on Eurasian oaks involving a fraction of these evergreen Asian species indicated similar patterns, highlighting the incongruence between morphology and phylogenetic relationships in Quercus (Denk and Grimm, 2010; Simeone et al, 2016). Prior morphological and phylogenetic studies have provided evidences that Section Heterobalanus is an expanded/natural group within Group Ilex (Zhou et al, 1995; Manos et al, 2001; Deng et al, 2017); however, a morphologically distinct species ( Quercus engleriana ) was found to be paraphyletic within the Heterobalanus clade in that phylogeny (Manos et al, 2001), and our phylogenetic implications of NJ trees also rejected the monophyly of Section Heterobalanus (Figure 3 and Figure S13) except for a NJ tree using the combination of ITS and SAP (Figure S12), which slightly supported the Heterobalanus subclade (BP = 58) within Group Ilex .…”

“…Oak species of the Group Quercus (morphology-based Section Quercus) are clearly distinct from the clade comprising oaks of Groups Cerris and Ilex , strongly supporting a scenario of two possible originations (the New World and Old World Oaks) of Quercus that was previously identified with phylogenetic classification (Oh and Manos, 2008; Denk and Grimm, 2009, 2010; Denk and Tekleva, 2014; Hubert et al, 2014). In China, the three deciduous East Asian species of Group Cerris (morphology-based Section Aegilops) are strongly supported forming a monophyletic clade in contrast to the shared “ Cerris - Ilex ” haplotype scenario found in some Eurasian oaks (Denk and Grimm, 2010; Hubert et al, 2014; Simeone et al, 2016). Pollen morphology of the three cerriod oaks in East Asia ( Q. acutissima, Q. variabilis , and Q. chenii ) is different from the evergreen oaks of Group Ilex in China (Cao and Zhou, 2002), thus suggesting possible reproductive isolation between the cerriod and ilicoid oaks in China.…”

“…Pollen morphology of the three cerriod oaks in East Asia ( Q. acutissima, Q. variabilis , and Q. chenii ) is different from the evergreen oaks of Group Ilex in China (Cao and Zhou, 2002), thus suggesting possible reproductive isolation between the cerriod and ilicoid oaks in China. However, although the hybrid formations are considered to be highly frequent among closely related species within a section/group, hybridization and gene flow between oak species from Groups Cerris and Ilex were found in Europe, such as hybridization between Quercus suber and Q. ilex , which may reflect enigmatic species evolutionary history of the two major Old World clades (Groups Cerris and Ilex ) linked with complex incidence of geographical effects during different periods in Europe (Aldrich and Cavender-Bares, 2011; Hubert et al, 2014; Simeone et al, 2016). Within Group Ilex , species of the morphological Sections Heterbalanus, Engleriana, and Echinolepides are mixed and form multiple clades without clear boundaries in the NJ trees (i.e., Figures 3 and Figure S13), albeit the oaks among the three morphology-based sections show distinct morphological differences in foliage and acorn cupule patterns (Pu et al, 2002; Peng et al, 2007).…”

Genetic Structure and Evolutionary History of Three Alpine Sclerophyllous Oaks in East Himalaya-Hengduan Mountains and Adjacent Regions

“…Generally, numerous studies have revealed shared DNA polymorphisms between closely related species or species complex (e.g., Du et al, 2009; Li et al, 2012; Simeone et al, 2016). This situation can be divided into two categories: firstly, retention of ancestral polymorphisms which caused by incomplete lineage sorting during and following speciation (Heckman et al, 2007; Wilyard et al, 2009); secondly, introgression or introgressive hybridization which caused by genetic exchange after secondary contact between previously geographically separated species (Liston et al, 1999; Gay et al, 2007).…”

Taxonomy and palaeoecology of two widespread western Eurasian Neogene sclerophyllous oak species: Quercus drymeja Unger and Q. mediterranea Unger

“…Species are distributed in temperate and subtropical regions; the northern limit of their distribution corresponds to the transition from snow climates with warm summers to snow climates with cool summers (Dfb to Dfc, and Dwb to Dwc climates according to the Köppen-Geiger classification; Kottek et al, 2006;Peel et al, 2007). Recent molecular phylogenetic and morphological studies recovered two well-supported main lineages within oaks, one comprising the white oaks (Quercus Group Quercus), red oaks (Quercus Group Lobatae) and golden-cup oaks (Quercus Group Protobalanus), whereas the other group comprises the cyclecup oaks (Quercus Group Cyclobalanopsis), the Cerris oaks (Quercus Group Cerris) and the Ilex oaks (Quercus Group Ilex; Denk and Grimm, 2010;Hubert et al, 2014;Hipp et al, 2015;Simeone et al, 2016). Quercus Groups Lobatae and Protobalanus are presently confined to North and Central America and Quercus Group Quercus occurs throughout the Northern Hemisphere, while Quercus Groups Ilex, Cerris and Cyclobalanopsis are Eurasian.…”