Plant Systematics and Evolution

, Volume 304, Issue 10, pp 1255–1267 | Cite as

Differentiation of the endemic Greek genus Hymenonema and its relatives of subtribe Scolyminae (Compositae, Cichorieae) based on a multilocus species tree reconstruction

  • Eleni Liveri
  • Salvatore Tomasello
  • Christian Hammerschmid
  • Georgia Kamari
  • Christoph Oberprieler
Original Article


Hymenonema (Compositae, tribe Cichorieae) together with the genera Catananche, Gundelia, and Scolymus forms the subtribe Scolyminae. It is endemic to Greece and consists of two species, Hymenonema laconicum and Hymenonema graecum, which occur in the south Peloponnisos and central Aegean area, respectively. The present contribution aims at a phylogenetic reconstruction of evolutionary relationships among the 12 species of the subtribe, focusing on the temporal and spatial framework for its evolution. The phylogenetic relationships among the members of Scolyminae were inferred from molecular data based on the multi-copy region of the nrDNA internal transcribed spacers ITS1 and ITS2, two intergenic spacers of the cpDNA (trnL-trnF, rpl32-trnL), and one single-copy nuclear region (D10). The gene trees were reconstructed using Bayesian phylogenetic methods. All gene trees support the monophyly of Hymenonema and the sister-group relationship with the genus Scolymus. The further sister-group relationship of this group (HymenonemaScolymus) with Catananche is also supported by nrDNA and cpDNA analyses. Finally, a species tree (inferred in a Bayesian coalescent framework) was reconstructed and dates the divergence time between the two Hymenonema species to the Pleistocene (around 1.3 Ma ago). Maximum likelihood-based biogeographical reconstructions suggest a Miocene (pre-Messinian) differentiation of the subtribe on the northern Tethyan platform, followed by Miocene/Pliocene dispersal events to the western Mediterranean and North-African platforms and final, small-scale vicariance events within the genera in the Pleistocene.


Aegean Asteraceae Biogeography Phylogeny Pleistocene Pliocene 



This research was supported by an Erasmus + for Traineeships Grant to E.L. in 2014–2015. The suggestions by two anonymous reviewers improved the present contribution considerably and are thankfully acknowledged.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interests.

Supplementary material

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  1. Blattner FR, Weising K, Bänfer G, Maschwitz U, Fiala B (2001) Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Molec Phylogen Evol 19:331–344. CrossRefGoogle Scholar
  2. Cellinese N, Smith SA, Edwards EJ, Kim ST, Haberle RC, Avramakis M, Donoghue MJ (2009) Historical biogeography of the endemic Campanulaceae of Crete. J Biogeogr 36:1253–1269. CrossRefGoogle Scholar
  3. Chapman MA, Chang J, Weisman D, Kesseli RV, Burke JM (2007) Universal markers for comparative mapping and phylogenetic analysis in the Asteraceae (Compositae). Theor Appl Genet 115:747–755. CrossRefPubMedGoogle Scholar
  4. Chatzimanolis S, Trichas A, Giokas S, Mylonas M (2003) Phylogenetic analysis and biogeography of Aegean taxa of the genus Dendarus (Coleaoptera: Tenebrionidae). Insect Syst Evol 34:3. CrossRefGoogle Scholar
  5. Comes HP, Tribsch A, Bittkau C (2008) Plant speciation in continental island floras as exemplified by Nigella in the Aegean archipelago. Philos Trans Roy Soc London B Biol Sci 363:3083–3096. CrossRefPubMedGoogle Scholar
  6. Darriba D, Taboada GL, Doallo R, Posada D (2015) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772. CrossRefGoogle Scholar
  7. Dimopoulos P, Raus T, Bergmeier E, Constantinidis T, Iatrou G, Kokkini S, Strid A, Tzanoudakis D (2013) Vascular plants of Greece. An annotated checklist (Englera 31). Botanischer Garten und Botanisches Museum Berlin-Dahlem, Hellenic Botanical Society, Berlin, AthensGoogle Scholar
  8. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15. CrossRefGoogle Scholar
  9. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec Biol Evol 29:1969–1973. CrossRefPubMedGoogle Scholar
  11. Enke N, Gemeinholzer B (2008) Babcock revisited: new insights into generic delimitation and character evolution in Crepis L. (Compositae: Cichorieae) from ITS and matK sequence data. Taxon 57:756–768Google Scholar
  12. Euro + Med (2006–2018) Euro + Med PlantBase—the information resource for Euro-Mediterranean plant diversity. Available at: Accessed Jan 2018
  13. Fattorini S (2002) Biogeography of the tenebrionid beetles (Coleoptera, Tenebrionidae) on the Aegean Islands (Greece). J Biogeogr 29:49–67. CrossRefGoogle Scholar
  14. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. CrossRefPubMedGoogle Scholar
  15. Gould SJ (2002) The structure of evolutionary theory. The Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  16. Greuter W (1979) The origins and evolution of island floras as exemplified by the Aegean Archipelago. In: Bramwell D (ed) Plants and Islands. Academic Press, New York, pp 87–106Google Scholar
  17. Heled J, Drummond AJ (2010) Bayesian inference of species tree from multilocus data. Molec Biol Evol 27:570–580. CrossRefPubMedGoogle Scholar
  18. Kendall DG (1948) On the generalized “birth-and-death” process. Ann Math Stat 19:1–15CrossRefGoogle Scholar
  19. Kilian N, Gemeinholzer B, Lack HW (2009) Cichoriae. In: Funk VA, Susanna A, Stuessy TF, Bayer RJ (eds) Systematics, evolution and biogeography of the compositae. IAPT, Vienna, pp 343–383Google Scholar
  20. Liveri L, Bareka P, Kamari G (2018) Taxonomic study on the Greek endemic genus Hymenonema (Asteraceae: Cichorieae), using morphological and karyological traits. Willdenowia 48:5–21. CrossRefGoogle Scholar
  21. Meulenkamp JE, Sissingh W (2003) Tertiary palaeogeography and tectonostratigraphic evolution of the Northern and Southern Peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeogr Palaeoclimatol Palaeoecol 196:209–228. CrossRefGoogle Scholar
  22. Oberprieler C, Zimmer C, Bog M (2018) Are there morphological and life-history traits under climate-dependent differential selection in S Tunisian Diplotaxis harra (Brassicaceae) populations? Ecol Evol 8:1047–1062. CrossRefPubMedGoogle Scholar
  23. Petrova G, Moyankova D, Nishii K, Forrest L, Tsiripidis I, Drouzas AD, Djilianov D, Möller M (2015) The European paleoendmic Haberlea rhodopensis (Gesneriaceae) has an Oligocene origin and a Pleistocene diversification and occurs in a long-persisting refugial area in southeastern Europe. Int J Pl Sci 176:499–514. CrossRefGoogle Scholar
  24. Poulakakis N, Kapli P, Lymberakis P, Trichas A, Vardinoyiannis K, Sfenthourakis S, Mylonas M (2015) A review of phylogeographic analyses of animal taxa from the Aegean and surrounding regions. J Zool Syst Evol Res 53:18–32. CrossRefGoogle Scholar
  25. Rambaut A, Drummond AJ (2007) Tracer v1.4: MCMC trace analyses tool. Available at: Accessed 1 Oct 2018
  26. Ree RH, Smith SA (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extrinction, and cladogenesis. Syst Biol 57:4–14. CrossRefPubMedGoogle Scholar
  27. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. CrossRefGoogle Scholar
  28. Ronquist F, Huelsenbeck J, Teslenko M (2011) Draft MrBayes version 3.2 manual: tutorials and model summaries. Available at: Accessed 1 Oct 2018
  29. Rydin C, Pedersen KR, Friis EM (2004) On the evolutionary history of Ephedra: Cretaceous fossils and extant molecules. Proc Natl Acad Sci USA 101:16571–16576. CrossRefPubMedGoogle Scholar
  30. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288. CrossRefGoogle Scholar
  31. Simmons M, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381CrossRefGoogle Scholar
  32. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods). Version 4.0.b10. Sinauer Associates, SunderlandGoogle Scholar
  33. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. CrossRefGoogle Scholar
  34. Thompson JD (2005) Plant evolution in the mediterranean. Oxford University Press, OxfordCrossRefGoogle Scholar
  35. Thompson J, Higgins D, Gibson T (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positionspecific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680CrossRefGoogle Scholar
  36. Tremetsberger K, Gemeinholzer B, Zetzsche H, Blackmore S, Kilian N, Talavera S (2013) Divergence time estimation in Cichorieae (Asteraceae) using a fossil-calibrated relaxed molecular clock. Organisms Diversity Evol 13:1–13. CrossRefGoogle Scholar
  37. Tremetsberger K, Ortiz MÁ, Terrab A, Balao F, Casimiro-Soriguer R, Talavera M, Talavera S (2016) Phylogeography above the species level for perennial species in a composite genus. AoB PLANTS 8:plv142. CrossRefGoogle Scholar
  38. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols. A guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  39. Wright JJ, David SR, Near TJ (2012) Gene trees, species trees, and morphology converge on a similar phylogeny of living gars (Actinopertygii: Holostei: Lepidosteidae), an ancient clade of ray-finned fishes. Molec Phylogenet Evol 63:848–856. CrossRefPubMedGoogle Scholar
  40. Xie W, Lewis PO, Fan Y, Kuo L, Chen MH (2011) Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 60:150–160. CrossRefPubMedGoogle Scholar
  41. Young ND, Healy J (2003) GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinform 4:6. CrossRefGoogle Scholar
  42. Yule GU (1924) A mathematical theory of evolution: based on the conclusions of Dr. J. C. Willis. Philos Trans Roy Soc London B Biol Sci 213:21–87. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology, Section of Plant BiologyUniversity of PatrasRioGreece
  2. 2.Evolutionary and Systematic Botany Group, Institute of Plant SciencesUniversity of RegensburgRegensburgGermany
  3. 3.Department of Systematics, Biodiversity and Evolution of Plants (with Herbarium), Albrecht-von-Haller-InstituteGeorg-August-University GöttingenGöttingenGermany

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