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Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock

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Abstract

Knowing the age of lineages is key to understanding their biogeographic history. We aimed to provide the best estimate of the age of Cichorieae and its subtribes based on available fossil evidence and DNA sequences and to interpret their biogeography in the light of Earth history. With more than 1,550 species, the chicory tribe (Cichorieae, Asteraceae) is distributed predominantly in the northern Hemisphere, with centres of distribution in the Mediterranean region, central Asia, and SW North America. Recently, a new phylogenetic hypothesis of Cichorieae based on ITS sequences has been established, shedding new light on phylogenetic relationships within the tribe, which had not been detected so far. Cichorieae possess echinolophate pollen grains, on the surface of which cavities (lacunae) are separated by ridges. These lacunae and ridges show patterns characteristic of certain groups within Cichorieae. Among the fossil record of echinolophate pollen, the Cichorium intybus-type is the most frequent and also the oldest type (22 to 28.4 million years old). By using an uncorrelated relaxed molecular clock approach, the Cichorieae phylogenetic tree was calibrated with this fossil find. According to the analysis, the tribe originated no later than Oligocene. The species-rich core group originated no later than Late Oligocene or Early Miocene and its subtribes diversified no later than Middle/Late Miocene or Early Pliocene—an eventful period of changing geological setting and climate in the Mediterranean region and Eurasia. The first dispersal from Eurasia to North America, which resulted in the radiation of genera and species in North America (subtribe Microseridinae), also occurred no later than Middle or Late Miocene, suggesting the Bering land bridge as the route of dispersal.

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Acknowledgements

We thank P. Hochuli (Zurich) for sharing information on Cichoraearumpollenites, S. Ho (Sydney) and G. Schneeweiss (Vienna) for help with the program BEAST, and A. Wortley (Edinburgh) for helpful discussion on Cichorieae pollen. The comments of two anonymous reviewers greatly improved the manuscript. We also acknowledge a Juan de la Cierva fellowship of the Ministerio de Educación y Ciencia (Spain) and the financial support of the European Commission’s Research Infrastructure Action via the SYNTHESYS Project (both to K.T.).

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Appendix

Appendix

ITS sequences used with their EMBL/GenBank accession numbers and voucher information including collector(s) and number and herbarium accession number (only for newly provided sequences). The DNA Bank Network number (http://www.dnabank-network.org/; Gemeinholzer et al. 2011) is indicated, if available.

Ingroup: Agoseris retrorsa (Benth.) Greene AJ633461 (Bachmann A71, GAT bg65); Andryala integrifolia L. AJ633384a; Arnoseris minima (L.) Schweigg. & Körte AJ633445 (Schuster s/n, GAT bg155); Catananche caerulea L. AJ633466 (Romania, Hortus Botanicus Universitatis Iasi: 265-53/02-18/36, GAT bg26); Chondrilla juncea L. AJ633348 (IPK-Gatersleben-Expedition: ITA-81 no. 7628, GAT bg20); Cicerbita alpina (L.) Wallr. AJ633324 (Blattner & Jakob BJ02-067, GAT bg96); Cichorium intybus L. AJ633451b; Crepis biennis L. AJ633355 (Czech Republic, BG Brno 84 9/03, GAT bg223); Gundelia tournefortii L. AY504691c; Helminthotheca comosa (Boiss.) Holub AJ633323 (Zidorn 23.01.2003a-1, GAT bg274); Helminthotheca echioides L. (Holub) AJ633321 (France, Jardin Botanique de Dijon 19-103/02, GAT bg128); Heteracia szovitsii Fisch. & C.A.Mey. AJ633283 (Newodowski s/n, GAT bg81); Hispidella hispanica Lam. AJ633432 (Pizarro & Navarro 2460, GAT bg199); Hymenonema graecum (L.) DC. EU436694 (Jäth s/n, B 100209163, DB 467); Hyoseris radiata L. AF528494d; Hypochaeris angustifolia (Litard. & Maire) Maire AJ627257e; Hypochaeris glabra L. AJ627264e; Hypochaeris laevigata (L.) Ces. & al. AJ627265e; Hypochaeris leontodontoides Ball AJ627266e; Hypochaeris maculata L. AF528454d; Hypochaeris oligocephala (Svent. & Bramwell) Lack AJ627268e; Hypochaeris patagonica Cabrera AM932283 (Essl 6202, WU 59780); Hypochaeris radicata L. AJ627270e; Hypochaeris sessiliflora Kunth AF528482d; Lactuca sativa L. AJ633337 (Romania, BG Cluj-Napoca 681-7/03, GAT bg207); Lasiospora hirsuta (Gouan) Cass. AJ633479 (France, BG Montpellier 774-101-28/03, GAT bg213); Launaea lanifera Pau EU436699 (Vogt 14455/Oberprieler 8764, B 100355175, DB 7038); Leontodon hispidus L. DQ451770f; Leontodon saxatilis Lam. AJ633317 (Egli, Leuenberger & Arroyo-Leuenberger 3137b, B, GAT bg112); Notoseris triflora (Hemsl.) C.Shih EU436698 (Li Heng 13455, CAS 1031382); Phitosia crocifolia (Boiss. & Heldr.) Kamari & Greuter EU436695 (Strid & Papanikolaos 15261, herb. Greuter); Picris hieracioides L. AJ633320 (Germany, BG Bremen 117-86/02, GAT bg127); Picris hispanica (Willd.) P. D. Sell DQ451808f; Pyrrhopappus grandiflorus (Nutt.) Nutt. AJ633459 (Bachmann B05, GAT bg68); Rafinesquia neomexicana A.Gray AF473613g; Rhagadiolus edulis Gaertn. AF528495d; Schlagintweitia intybacea (All.) Griseb. AJ633426a; Scolymus hispanicus L. AJ633470 (Germany, Berlin, Arboretum Späth s/n, GAT bg25); Scorzonera hispanica L. AJ633472 (Denmark, BG Hauniensis 429-130-149/01, GAT bg12); Scorzonera suberosa K.Koch AY508199h; Scorzoneroides autumnalis (L.) Moench AF528486d; Scorzoneroides helvetica (Mérat) Holub DQ451767f; Sonchus oleraceus L. AJ633306 (Ochsmann 8192, GAT bg117); Soroseris glomerata (Decne.) Stebbins EU436696 (T.-N. Ho 1692, CAS 939054); Taraxacum officinale F.H.Wigg. L48337, L48338i; Tolpis barbata (L.) Gaertn. AJ633434 (France, Jardin Botanique de Dijon 19-229-103/02, GAT bg58); Tragopogon porrifolius L. AJ633496 (Romania, BG Cluj-Napoca 759 7/03, GAT bg219); Warionia saharae Benth. & Coss. AY190608 (Morocco, Lippat 25346, US)j; Willemetia stipitata (Jacq.) Dalla Torre EU436697 (Greece, Willing 11335, B 100209153, DB 462).

Outgroup: Barnadesia arborea Kunth AF412883k; Brachylaena discolor DC. AY826236l; Cardopatium corymbosum (L.) Pers. AY826238l; Echinops exaltatus Schrad. AY538649m; Ericentrodea corazonensis (Hieron.) S.F.Blake & Sherff AY429088n; Ericentrodea decomposita S.F.Blake & Sherff AY429089n; Geigeria ornativa O.Hoffm. U84774o; Gerbera crocea Kuntze AY504687b; Heterolepis aliena (L.f.) Druce AY504700b; Mutisia grandiflora Humb. & Bonpl. AF546081p; Oldenburgia intermedia P.Bond AY826303l; Pluchea indica (L.) Less. AF430795q; Saussurea maximowiczii Herder AY826324l; Schlechtendalia luzulifolia Less. AF412836k.

a Fehrer et al. (2007); b Gemeinholzer & Bachmann (2005); c Funk et al. (2004); d Samuel et al. (2003); e Tremetsberger et al. (2005); f Samuel et al. (2006); g Lee et al. (2002); h Mavrodiev et al. (2004); i Kim et al. (1996); j J.L. Panero (unpublished data); k Gustaffson et al. (2001); l Susanna et al. (2006); m Garnatje et al. (2005); n Kimball & Crawford (2004); o Eldenäs et al. (1998); p H.-G. Kim (unpublished data); q C.H. Chou & F.T. Huang (unpublished data).

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Tremetsberger, K., Gemeinholzer, B., Zetzsche, H. et al. Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. Org Divers Evol 13, 1–13 (2013). https://doi.org/10.1007/s13127-012-0094-2

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