Plastome data reveal multiple geographic origins of Quercus Group Ilex.

Marco Cosimo Simeone,Alain Franc,Thomas Denk,Federico Vessella,Alessio Papini,Simone Cardoni,Guido W Grimm,Enrico Tordoni,Roberta Piredda

doi:10.7717/peerj.1897

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.

Highlights

Quercus L. is among the most ecologically diverse and economically important extratropical tree genera in the northern hemisphere (Kubitzki, 1993)
If we accept the monophyly of the genus Quercus, which is further supported by morphology and evidence from the fossil record, haplotypes of Castanea/Castanopsis and Notholithocarpus that group with the ‘New World’ and ‘Old World’ oaks, respectively, can only be the result of incomplete lineage sorting during the formation of the modern genera and/or ancestral gene flow between early diverged lineages
In the case of woody angiosperms with a subtropical to temperate distribution such as e.g., Nothofagaceae (Svenson et al, 2001; Knapp et al, 2005), Rhus (Yi, Miller & Wen, 2004), Cornus (Xiang et al, 2005), Carpinus (Yoo & Wen, 2007), Castanea (Lang et al, 2007), Juglans (Aradhya et al, 2007), and Carya (Zhang et al, 2013a), this approach runs the risk of capturing but a limited aspect of the evolutionary history of the focal group

Summary

Introduction

Quercus L. (oaks) is among the most ecologically diverse and economically important extratropical tree genera in the northern hemisphere (Kubitzki, 1993). (oaks) is among the most ecologically diverse and economically important extratropical tree genera in the northern hemisphere (Kubitzki, 1993). Species diversity is highest in the Americas (Groups Quercus, Lobatae and Protobalanus; Flora of North America Editorial Committee, 1997) and Southeast Asia and southern China (Group Cyclobalanopsis; Flora of China Editorial Committee, 1999). A relatively lower number of species occurs in western Eurasia and the Mediterranean (Groups Ilex and Cerris; Kubitzki, 1993; Menitsky, 2005). The northern limit of oaks in North America and Eurasia coincides with the border of Dfb to Dfc and Dwb to Dwc climates, snow climates with warm versus cool summers (Köppen, 1936; Kottek et al, 2006; Peel, Finlayson & McMahon, 2007)

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