Plastome data reveal multiple geographic origins of Quercus Group 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 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. Main plastid haplotypes shared by distinct oak lineages from the same geographic region and high plastid diversity in members of Group Ilex are indicative for a polyphyletic origin of their plastomes. The results suggest that incomplete lineage sorting and repeated phases of unidirectional 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.

Remarkably conserved plastid genomes of Quercus group Cerris in China: comparative and phylogenetic analyses

“…The size, gene content, gene order, and GC content of the two newly generated plastid genomes resembled those of Q . variabilis (Yang et al ).…”

“…Reference‐guided assembly was then used to reconstruct the plastid genomes with the programs MIRA 4.0.2 (Chevreux et al 2004) and MITObim v1.7 (Hahn et al ). In this process, the plastid genomes of Quercus aliena (KU240007) (Yang et al ), Quercus rubra (JX970937) (Alexander and Woeste ) and Castanea mollissima (HQ336406) (Jansen et al 2011) were used as reference genomes. The complete plastid genome sequence was imported into the program DOGMA for annotation (Wyman et al 2004), followed by manual correction through comparison with other published Fagaceae plastomes in GENEIOUS R8.…”

“…In terms of evolutionary studies, Cerris has been less intensively studied than other groups of oaks. The relationships of Cerris have only been explored in the phylogenetic studies of the whole genus and inferred from a few plastid or nuclear markers (Manos et al , Manos et al 2001, Denk and Grimm , Hubert et al , Simeone et al ). Considering the widespread adoption of next generation sequencing (lower cost and time saving) and the advantages of the plastome (non‐recombinant, uniparental inheritance, and a smaller effective population size), it is feasible to explore Cerrris at the level of complete plastid genome.…”

East Asian origins of European holly oaks (Quercus section Ilex Loudon) via the Tibet‐Himalaya

“…The origin and evolution of Quercus section Ilex have long been a focus of systematists and biogeographers (Axelrod, ; Manos, Zhou, & Cannon, ; Simeone et al, ; Zhou, ). The central controversy has been whether Quercus section Ilex originated in Europe or in Asia.…”

“…Quercus section Ilex Loudon is an ecologically diverse lineage with about 35 species widely distributed in Mediterranean Europe, Northern Africa and the East Asian subtropics. The section exemplifies the East Asian‐Tethyan disjunction (Figure ) (Simeone et al, ). Trees of section Ilex are keystone elements of Mediterranean savannas (e.g.…”