Plastome data reveal multiple geographic origins of Quercus Group Ilex - PubMed
- ️Fri Jan 01 2016
Plastome data reveal multiple geographic origins of Quercus Group Ilex
Marco Cosimo Simeone et al. PeerJ. 2016.
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.
Keywords: Ancient introgression; Decoupled phylogenies; Fagaceae; Incomplete lineage sorting; Mediterranean.
Conflict of interest statement
The authors declare there are no competing interests.
Figures

ML tree of plastid accessions; tentatively rooted with the Notholithocarpus-Chrysolepis subtree. Stars indicate subtrees comprising accessions of Mediterranean members of Quercus Group Ilex. Colouration refers to the taxonomic affiliations and main clades of specimens. Number at branches indicate non-parametric bootstrap support under maximum likelihood using two different implementations and posterior probabilities calculated using Bayesian inference.

Haplotype network based on length-conserved portions of the trnH-psbA spacer. Colouration refers to the taxonomic affiliation of specimens.

Geographic pattern of plastid haplotype variation in Mediterranean members of Quercus Group Ilex. (A) Map showing the taxonomic identity of sampled specimens. (B) Map showing the plastid haplotypes of sampled specimens.

Mapping of chloroplast evolution in oaks (using the same rooting scenario as in Fig. 1) on current evolutionary synopsis (based on nuclear sequence data, morphology, and the fossil record; modified after Grímsson et al. (, Fig. 16). Colouring of the plastid lineages refers to branches/subclades in Fig. 1: bluish, common (ancestral) and ‘New World’ oak/castanoids plastid haplotype lineages; green, lineages of the unique ‘Euro-Med’ plastid haplotype found only in Mediterranean members of Group Ilex; reddish, lineages of ‘Old World’ oaks and Eurasian castanoids. Note that members of Group Ilex keep plastid haplotypes of five different evolutionary sources/systematic affinities. Abbreviations: C, Cretaceous; Pa, Paleocene; E, Eocene; O, Oligocene; M, Miocene; Pl, Plio-/Pleistocene.

Eocene set-up and the origin of the ‘Euro-Med’ haplotype. (A) Unequivocal fossil record of oaks in the Eocene mapped on a palaeotopographic map highlighting a primary split into a high-latitude and mid-latitude lineage that likely correspond to the deep phylogenetic split seen in nuclear and plastid sequence data of modern oaks between the ‘New World Clade’ (Groups Protobalanus, Quercus and Lobatae) and the ‘Old World Clade’ (Groups Cyclobalanopsis, Ilex, Cerris). (B–C) Scenarios that can explain the occurrence of the unique ‘Euro-Med’ haplotype in westernmost members of Quercus Group Ilex. (B) The ‘Euro-Med’ haplotype belonged to an extinct oak lineage geographically/biologically separated from both the ancestors of the New World and Old World Clade. Westward expansion of Himalayan members of Group Ilex and subsequent large-scale introgression/hybridisation homogenised the western members of Group Ilex and the extinct oak lineage, retaining and evolving the original haplotype in the Mediterranean region. (C) The ‘Euro-Med’ haplotype reflects geographic fragmentation within the Paleogene range of the Old World Clade that was overprinted to some degree after later radiation phases of Group Ilex. Palaeotopographic map base used with permission from Ron Blakey, © Colorado Plateau Geosystems.

Tectonic activity during the Eocene and past and modern distribution of the New World (white) and Old World (yellow) groups within Quercus. Black lines indicate major subduction zones, red lines major orogenies. Note that the high latitude lineage of oaks (Quercus Group Lobatae, Group Quercus, Group Protobalanus) evolved in tectonically stable regions, whereas the low latitude lineage (Quercus Group Ilex, Group Cyclobalanopsis, Group Cerris) evolved in tectonically unstable regions. Uppercase and lowercase letters refer to extant and extinct distribution areas of major oak lineages: P,p, Group Protobalanus; Q,q, Group Quercus; L,l, Group Lobatae; I,i, Group Ilex; C,c, Group Cerris; Y,y, Group Cyclobalanopsis. Palaeotopographic map base used with permission from Ron Blakey, © Colorado Plateau Geosystems.
Similar articles
-
Yang J, Vázquez L, Chen X, Li H, Zhang H, Liu Z, Zhao G. Yang J, et al. Front Plant Sci. 2017 May 19;8:816. doi: 10.3389/fpls.2017.00816. eCollection 2017. Front Plant Sci. 2017. PMID: 28579999 Free PMC article.
-
Yang Y, Zhou T, Qian Z, Zhao G. Yang Y, et al. Genomics. 2021 May;113(3):1438-1447. doi: 10.1016/j.ygeno.2021.03.013. Epub 2021 Mar 17. Genomics. 2021. PMID: 33744343
-
Simeone MC, Cardoni S, Piredda R, Imperatori F, Avishai M, Grimm GW, Denk T. Simeone MC, et al. PeerJ. 2018 Oct 17;6:e5793. doi: 10.7717/peerj.5793. eCollection 2018. PeerJ. 2018. PMID: 30356975 Free PMC article.
-
Maldonado-Alconada AM, Castillejo MÁ, Rey MD, Labella-Ortega M, Tienda-Parrilla M, Hernández-Lao T, Honrubia-Gómez I, Ramírez-García J, Guerrero-Sanchez VM, López-Hidalgo C, Valledor L, Navarro-Cerrillo RM, Jorrin-Novo JV. Maldonado-Alconada AM, et al. Int J Mol Sci. 2022 Sep 1;23(17):9980. doi: 10.3390/ijms23179980. Int J Mol Sci. 2022. PMID: 36077370 Free PMC article. Review.
-
Rey MD, Castillejo MÁ, Sánchez-Lucas R, Guerrero-Sanchez VM, López-Hidalgo C, Romero-Rodríguez C, Valero-Galván J, Sghaier-Hammami B, Simova-Stoilova L, Echevarría-Zomeño S, Jorge I, Gómez-Gálvez I, Papa ME, Carvalho K, Rodríguez de Francisco LE, Maldonado-Alconada AM, Valledor L, Jorrín-Novo JV. Rey MD, et al. Int J Mol Sci. 2019 Feb 6;20(3):692. doi: 10.3390/ijms20030692. Int J Mol Sci. 2019. PMID: 30736277 Free PMC article. Review.
Cited by
-
Framework Phylogeny, Evolution and Complex Diversification of Chinese Oaks.
Yang J, Guo YF, Chen XD, Zhang X, Ju MM, Bai GQ, Liu ZL, Zhao GF. Yang J, et al. Plants (Basel). 2020 Aug 13;9(8):1024. doi: 10.3390/plants9081024. Plants (Basel). 2020. PMID: 32823635 Free PMC article.
-
A chromosome-level genome assembly of the Chinese cork oak (Quercus variabilis).
Han B, Wang L, Xian Y, Xie XM, Li WQ, Zhao Y, Zhang RG, Qin X, Li DZ, Jia KH. Han B, et al. Front Plant Sci. 2022 Sep 23;13:1001583. doi: 10.3389/fpls.2022.1001583. eCollection 2022. Front Plant Sci. 2022. PMID: 36212310 Free PMC article.
-
Yan M, Liu R, Li Y, Hipp AL, Deng M, Xiong Y. Yan M, et al. BMC Evol Biol. 2019 Nov 4;19(1):202. doi: 10.1186/s12862-019-1523-z. BMC Evol Biol. 2019. PMID: 31684859 Free PMC article.
-
Yang Y, Zhu J, Feng L, Zhou T, Bai G, Yang J, Zhao G. Yang Y, et al. Front Plant Sci. 2018 Feb 1;9:82. doi: 10.3389/fpls.2018.00082. eCollection 2018. Front Plant Sci. 2018. PMID: 29449857 Free PMC article.
-
Comparative analysis of plastid genomes within the Campanulaceae and phylogenetic implications.
Li CJ, Wang RN, Li DZ. Li CJ, et al. PLoS One. 2020 May 14;15(5):e0233167. doi: 10.1371/journal.pone.0233167. eCollection 2020. PLoS One. 2020. PMID: 32407424 Free PMC article.
References
-
- Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control. 1974;19:716–723. doi: 10.1109/TAC.1974.1100705. - DOI
-
- Aradhya MK, Potter D, Gao F, Simon CJ. Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective. Tree Genetics and Genomes. 2007;3:363–378. doi: 10.1007/s11295-006-0078-5. - DOI
-
- Arnold ML. Evolution through genetic exchange. Vol. 3. Oxford: Oxford University Press; 2006.
-
- Barbero M, Bonin G, Loisel R, Quezel P. Changes and disturbances of forest ecosystems caused by human activities in the western part of the Mediterranean Basin. Vegetatio. 1990;87:151–173. doi: 10.1007/BF00042952. - DOI
Grants and 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.
LinkOut - more resources
Full Text Sources
Other Literature Sources
Miscellaneous