Plastome data reveal multiple geographic origins of Quercus Group Ilex
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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.
Cite this as
2015. Plastome data reveal multiple geographic origins of Quercus Group Ilex. PeerJ PrePrints 3:e1615v1 https://doi.org/10.7287/peerj.preprints.1615v1Author comment
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Supplemental Information
Plastome divergence in Fagales
Intra- and intertaxonomic minimum and maximum pairwise genetic distances in Fagales based on the used plastid markers
RbcL and trnK-matK haplotype networks
haplotype networks of the investigated dataset based on rbcL and trnK-matK markers
Additional Information
Competing Interests
The authors declare that they have no competing interests.
Author Contributions
Marco Cosimo Simeone conceived and designed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
Guido W Grimm conceived and designed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
Alessio Papini analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.
Federico Vessella analyzed the data, reviewed drafts of the paper.
Simone Cardoni performed the experiments, analyzed the data.
Enrico Tordoni performed the experiments, analyzed the data.
Roberta Piredda analyzed the data, contributed reagents/materials/analysis tools.
Alain Franc analyzed the data, wrote the paper, reviewed drafts of the paper.
Thomas Denk analyzed the data, wrote the paper, reviewed drafts of the paper.
DNA Deposition
The following information was supplied regarding the deposition of DNA sequences:
All sequence data generated as part of this study are available on GenBank (http://www.ncbi.nlm.nih.gov/genbank/)under accession numbers LM652969-LM653098; other relevant data are within the paper and its Supplementary files.
Data Deposition
The following information was supplied regarding data availability:
Primary data and analyses are provided for anonymous download at www.palaeogrimm.org/data/Smn15_OSA.zip
Funding
This project was funded by a Swedish Research Council (VR) grant to TD. GWG is financed by the Austrian Science Fund (FWF), grant M-1751-B16. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.