Skip to main content
Log in

Reticulate evolution of the critical Mediterranean Gagea sect. Didymobulbos (Liliaceae) and its taxonomic implications

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The genus Gagea Salisb. is the largest amongst Liliaceae, including 50–300 species. This genus can be subdivided into at least 14 sections: among them, there is the species-rich, relatively late-branching monophyletic sect. Didymobulbos. Most of species and putative hybrids within this section were included in this study for a total of about 148 accessions (corresponding to 35 taxa), almost all collected across the Euro-Mediterranean area. Thirty-seven morpho-anatomical and ontogenetic characters were considered, together with the cpDNA (trnL–trnF IGS, psbA–trnH IGS) and nrDNA (ITS region) molecular markers. Bayesian analysis revealed the phylogenetic relationships among Didymobulbos taxa, allowing us to demonstrate new circumscriptions of critical species complexes, such as those of G. chrysantha Schult. & Schult.f., G. dubia A. Terracc. and G. granatellii (Parl.) Parl. Also the prominent role played in this section by reticulate evolution is further highlighted: many taxa, often unexpectedly, are inferred to represent hybrids (31 % of investigated taxa). The division into series cannot be maintained as we found extensive molecular evidence of hybridization between them. A new taxonomic setting for Gagea sect. Didymobulbos is proposed, and five new species are described.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Burdet HM, Charpin A, Jacquemoud F (1982) Index Boissierianus Hispanicus. Candollea 37(2):397–427

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  PubMed  CAS  Google Scholar 

  • Davlianidze MT (1976) In: Mecniereba (ed), Kavkazskie predstaviteli roda Gagea Salisb. Tblilisi, pp 170

  • Durieu De Maisonneuve MC (1847–1849) Atlas de la Flore d’Algérie ou Illustrations d’un Grand Nombre de Plantes Nouvelles ou Rares de ce Pays, choisies surtout parmi celles qui ont été recuillies par les soins de la Commission scientifique de 1839 à 1844. Imprimerie Impériale, Paris

  • ESRI (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands

    Google Scholar 

  • Ferrer Gallego PP, Laguna Lumbreras E, Alba Villegas L, Tison J-M (2007) Sobre la presencia de Gagea lacaitae A. Terracc. (Liliaceae) en la flora valenciana. Acta Bot Malacitana 32:1–12

    Google Scholar 

  • Gargano D, Peruzzi L, Caparelli KF, Cesca G (2007) Preliminary observations on the reproductive strategies in five early-flowering species of Gagea Salisb. (Liliaceae). Bocconea 21:349–358

    Google Scholar 

  • Gomez-Zurita J, Vogler AP (2006) Testing introgressive hybridization hypotheses using statistical network analysis of nuclear and cytoplasmic haplotypes in the leaf beetle Timarcha goettingensis species complex. J Mol Evol 62:421–433

    Article  PubMed  CAS  Google Scholar 

  • Gurushidze M, Fritsch RM, Blattner FR (2010) Species-level phylogeny of Allium subgenus Melanocrommyum: Incomplete lineage sorting, hybridization and trnF gene duplication. Taxon 59:829–840

    Google Scholar 

  • Gutiérrez Esteban M, Vázquez Pardo FM (2010) Gagea fragifera. In: Marhold K (ed) IAPT/IOPB chromosome data 9. Taxon 59: 1300, E7

  • Gutiérrez Esteban M, Vázquez Pardo FM (2011) Gagea extremadurensis sp. nov. (Liliaceae) nueva espece del SW de la Península Ibérica. Folia Bot Extremadur 5:45–61

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harpke D, Peterson A (2008a) 5.8S motifs for the identification of pseudogenic ITS regions. Botany 86:300–305

    Article  CAS  Google Scholar 

  • Harpke D, Peterson A (2008b) Extensive 5.8S nrDNA polymorphism in Mammillaria (Cactaceae) with special reference to the identification of pseudogenic ITS regions. J Pl Res 121:261–270

    Article  CAS  Google Scholar 

  • Heyn CC, Dafni A (1977) Studies in the genus Gagea (Liliaceae) II. The non-platyspermous species from the Galilee, the Golan Heights and Mt. Hermon. Israel J Bot 26:11–22

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2002) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314

    Article  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Jakab G, Molnár AV (2011) First record of Gagea szovitsii in Central Europe. Biologia (Bratislava) 66(3):433–438

    Article  Google Scholar 

  • Jakob SS, Blattner FR (2006) A chloroplast genealogy of Hordeum (Poaceae): long-term persisting haplotypes, incomplete lineage sorting, regional extinction, and the consequences for phylogenetic inference. Mol Biol Evol 23:1602–1612

    Article  PubMed  CAS  Google Scholar 

  • Levichev IG (1990) The synopsis of the genus Gagea (Liliaceae) from the western Tien-Shan. Bot Zhurn 75(2):225–234

    Google Scholar 

  • Levichev IG (1999a) Phytogeographical analysis of the genus Gagea Salisb. (Liliaceae). Komarovia 1:47–59

    Google Scholar 

  • Levichev IG (1999b) The morphology of Gagea Salisb. (Liliaceae) I. Subterranean organs. Flora 194:379–392

    Google Scholar 

  • Levichev IG (2006) A review of the Gagea (Liliaceae) species in the flora of Caucasus. Bot Zhurn 91(6):917–951

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Marques I, Nieto Feliner G, Draper Munt D, Martins-Loução MA, Fuertes Aguilar J (2010) Unraveling cryptic reticulate relationships and the origin of orphan hybrid disjunct populations in Narcissus. Evolution 64(8):2353–2368

    PubMed  Google Scholar 

  • Martinoli G (1950) Studio cariologico della Gagea soleirolii F. Schultz. Caryologia 3(1):72–78

    Google Scholar 

  • Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala Univ, Uppsala

    Google Scholar 

  • Parlatore F (1839) Nova Ornithogali species ex naturali Liliacearum familia. L’Occhio 2(11):85–86

    Google Scholar 

  • Pascher AA (1906) Zur Kenntnis zweier mediterraner Arten der Gattung Gagea (Gagea foliosa R. Sch., Gagea peduncularis Pasch.). Beih Bot Centr 20(2):76–107

    Google Scholar 

  • Peruzzi L (2003) Contribution to the cytotaxonomical knowledge of Gagea Salisb. (Liliaceae) sect. Foliatae A. Terracc. and synthesis of karyological data. Caryologia 56(1):115–128

    Article  Google Scholar 

  • Peruzzi L (2008a) Hybridity as a main evolutionary force in the genus Gagea Salisb. (Liliaceae). Plant Biosyst 142(1):179–183

    Article  Google Scholar 

  • Peruzzi L (2008b) Contribution to the cytotaxonomical knowledge of the genus Gagea Salisb. (Liliaceae). III. New karyological data from the central Mediterranean area. Caryologia 61(1):92–106

    Google Scholar 

  • Peruzzi L (2012a) Nomenclatural novelties at sectional level in Gagea (Liliaceae). Atti Soc Tosc Sci Nat Mem ser B 118(2011):23–24

    Google Scholar 

  • Peruzzi L (2012b) Chromosome diversity and evolution in Gagea (Liliaceae). Bocconea 24:147–158

    Google Scholar 

  • Peruzzi L (2012c) Numeri Cromosomici per la Flora Italiana: 1490–1492. Inform Bot Ital 44(2):388–390

  • Peruzzi L, Aquaro G (2005) Contribution to the cytotaxonomical knowledge of Gagea Salisb. (Liliaceae). II. Further karyological studies on Italian populations. Candollea 60(1):237–253

    Google Scholar 

  • Peruzzi L, Bartolucci F (2006) Gagea luberonensis J.-M. Tison (Liliaceae) new for the Italian flora. Webbia 61:1–12

    Google Scholar 

  • Peruzzi L, Caparelli KF (2007) Gagea peduncularis (J. & C. Presl) Pascher (Liliaceae) new for the Italian flora. Webbia 62(2):261–268

    Google Scholar 

  • Peruzzi L, Tison J-M (2004) Typification and taxonomic status of eleven taxa of Gagea Salisb. (Liliaceae) described by Achille and Nicola Terracciano and conserved at Napoli (NAP). Candollea 59(2):325–346

    Google Scholar 

  • Peruzzi L, Tison J-M (2005) Typification and taxonomic status of six taxa of Gagea Salisb. (Liliaceae) described from Sicily and conserved at Palermo (PAL). Candollea 60(2):289–298

    Google Scholar 

  • Peruzzi L, Tison J-M (2007) Typification of six critical Mediterranean Gagea Salisb. (Liliaceae) taxa. Candollea 62(2):173–188

    Google Scholar 

  • Peruzzi L, Peterson A, Tison J-M, Peterson J (2008a) Phylogenetic relationships of Gagea Salisb. (Liliaceae) in Italy, inferred from molecular and morphological data matrices. Pl Syst Evol 276(3–4):219–234

    Article  Google Scholar 

  • Peruzzi L, Tison J-M, Peterson A, Peterson J (2008b) On the phylogenetic position and taxonomic value of Gagea trinervia (Viv.) Greuter and G. sect. Anthericoides A. Terracc. (Liliaceae). Taxon 57(4):1201–1214

    Google Scholar 

  • Peruzzi L, Leitch IJ, Caparelli KF (2009a) Chromosome diversity and evolution in Liliaceae. Ann Bot (London) 103:459–475

    Article  CAS  Google Scholar 

  • Peruzzi L, Scuderi L, Raimondo FM (2009b) Distribution of the genus Gagea (Liliaceae) in Sicily. Flora Medit 19:25–47

    Google Scholar 

  • Peruzzi L, Gestri G, Pierini B (2011a) Distribution of the genus Gagea (Liliaceae) in Sardinia. Flora Medit 21:261–272

    Google Scholar 

  • Peruzzi L, Peterson A, Tison J-M, Harpke D (2011b) New light on phylogeny and taxonomy of the Eurasian Gagea villosaG. fragifera complex (Liliaceae). Nord J Bot 29:722–733

    Article  Google Scholar 

  • Peterson A, John H, Koch E, Peterson J (2004) A molecular phylogeny of the genus Gagea (Liliaceae) in Germany inferred from non-coding chloroplast and nuclear DNA sequences. Pl Syst Evol 245:145–162

    Article  CAS  Google Scholar 

  • Peterson A, Levichev IG, Peterson J (2008) Systematics of Gagea and Lloydia (Liliaceae) and infrageneric classification of Gagea based on molecular and morphological data. Mol Phylogenet Evol 46:446–465

    Article  PubMed  CAS  Google Scholar 

  • Peterson A, Harpke D, Peruzzi L, Levichev IG, Tison J-M, Peterson J (2009) Hybridization drives speciation in Gagea (Liliaceae). Pl Syst Evol 278(3–4):133–148

    Article  CAS  Google Scholar 

  • Peterson A, Harpke D, Peruzzi L, Tison J-M, John H, Peterson J (2010) Gagea bohemica (Liliaceae), a highly variable monotypic species within sect. Didymobulbos. Plant Biosyst 144:308–322

    Article  Google Scholar 

  • Peterson A, Levichev IG, Peterson J, Harpke D, Schnittler M (2011) New insights into the phylogeny and taxonomy of Chinese species of Gagea (Liliaceae)—speciation through hybridization. Org Div Evol 11:387–407

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest, testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Rix EM (1984) Gagea Salisb. In: Davis PH (ed) Flora of Turkey 8: 312–327. Edinburgh University Press, Scotland

    Google Scholar 

  • Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am J Bot 84:1120–1136

    Article  PubMed  CAS  Google Scholar 

  • Stroh G (1937) Die Gattung Gagea Salisb. Beih Bot Centr 57B:485–520

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusets

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tison J-M (1996) Le Gagea du Petit Luberon. Monde Pl 455:17

    Google Scholar 

  • Tison J-M (1998) Note complementaire sur quelques Gagea français. Monde Pl 462:7–8

    Google Scholar 

  • Tison J-M (2001) Typification de Gagea cossoniana Pascher, de Gagea fragifera (Vill.) Ehr. Bayer & G. López et de Gagea maroccana (A. Terracc.) Sennen & Mauricio. Candollea 56:197–202

    Google Scholar 

  • Tison J-M (2004) Gagea polidorii J.-M. Tison, espèce méconnue du sud-ouest des Alpes et des Apennins. Acta Bot Gallica 151(3):319–326

    Google Scholar 

  • Tison J-M (2009) An update of the genus Gagea Salisb. (Liliaceae) in the Iberian Peninsula. Lagascalia 29:7–22

    Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Zarrei M, Wilkin P, Fay MF, Ingrouille MJ, Zarre S, Chase MW (2009) Molecular systematics of Gagea and Lloydia (Liliaceae; Liliales): implications of analyses of nuclear ribosomal and plastid sequences for infrageneric classification. Ann Bot 104:125–142

    Article  PubMed  CAS  Google Scholar 

  • Zarrei M, Wilkin P, Ingrouille MJ, Zarre S (2010) The systematic importance of anatomical data in Gagea (Liliaceae) from Flora Iranica area. Bot J Linn Soc 164:155–177

    Article  Google Scholar 

  • Zarrei M, Wilkin P, Ingrouille MJ, Chase MW (2011a) A revised infrageneric classification for Gagea Salisb. (Tulipeae; Liliaceae): insights from DNA sequence and morphological data. Phytotaxa 15:44–56

    Google Scholar 

  • Zarrei M, Wilkin P, Chase MW (2011b) Gagea Salisb. (Liliaceae) in Iran: an updated species checklist. Phytotaxa 15:33–43

    Google Scholar 

  • Zarrei M, Wilkin P, Ingrouille MJ, Leitch IJ, Buerki S, Fay MF, Chase MW (2012) Speciation and evolution in the Gagea reticulata species complex (Tulipeae; Liliaceae). Mol Phylogenet Evol 62:624–639

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Financial funding (EX60 %) from the University of Pisa is gratefully acknowledged. We would like to thank Erich Pasche and Helmut Kerndorff for providing some Gagea material from Turkey. We thank F.R. Blattner (Leibniz Isntitute of Plant Genetics and Crop Plant Research, Gatersleben, Germany) for helpful comments on the manuscript and A. Harpke for providing the distribution map.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lorenzo Peruzzi.

Appendix

Appendix

Sources of the studied material and EMBL/NCBI accession numbers. Taxon: Acronym: Origin (altitude a.s.l.): Voucher: trnL–trnF IGS, psbA–trnH IGS, ITS1 + 5.8SrDNA + ITS2 (#outgroup sequences taken from EMBL/NCBI). Acronyms of putative hybrids are marked with an asterisk.

Gagea algeriensis Chabert: ALG*: Morocco, Oujda, Jerada (1300 m): HAL 108486: HE649596, HE649692, HE649505. G. amblyopetala Boiss. & Heldr.: AMB1: Greece, Evritania-Gardiki (1,100 m): HAL 107892: HE649597, HE649693, HE649506; AMB2: Greece, Evvoia-Steni, à proximité du col des Monts Dirphys (1,400 m): HAL 107891: HE649598, HE649694, HE649507; AMB3: Italy, Sicily, Iblei, Monte Lauro (950 m): HAL 107890: HE649599, HE649695, HE649508. G. apulica Peruzzi & J.-M.Tison: APU1: France, Martigues, plateau de Bonnieu (10 m): HAL 107902: HE649600, HE649696, HE649509; APU2: Italy, Apulia, Lesina (5 m): CLU 12697: AM283111, AM409348, AM903046; APU3: Italy, Apulia, Murge, S. Simone, Taranto (241 m): CLU 18172: HE649601, HE649697, HE649510; APU4: Italy, Apulia, Murge, S. Simone, Taranto (241 m): CLU 18173: HE649602, HE649698, HE649511; APU5: Italy, Sicily, Campobello di Mazara, Trapani (25 m): PI s.n.: HE649603, HE649699, HE649512; APU6: Italy, Sicily, San Vito Lo Capo, Trapani (180 m): PI s.n.: HE649604, HE649700, HE649513. G. bohemica (Zauschn.) Schult. & Schult.f.: BOH1: Czech Republik, Moravia, Ivančice near Brno (230 m): HAL 095842: AJ419161, AJ416370, AJ427549; BOH2: Germany, Saxony-Anhalt, Ostrau (95 m): HAL 095849: FM204911, AJ416371, AJ437198; BOH3: Greece, Crete, near Ideon Andron (1,600 m): HAL 101645: AM161469, AM161463, AM265528; BOH4: Italy, Abruzzo, Gran Sasso (1,100 m): CLU 14925: AM265600, AM282987, AM287271; BOH5: Russia, Dagestan HAL 101787: AJ969117, AM085142, AM162672; BOH6: Spain, Orihvela del Tremedal/Tervel (1,700 m): HAL 107869: HE649605, HE649701, HE649514; BOH7: Turkey, W, near Yatagan (1,200 m): HAL 108495: HE649606, HE649702, HE649515; BOH8: Turkey, W, near Milas (800 m): HAL 108494: HE649607, HE649703, HE649516. G. chabertii A.Terracc.: CHA: Algeria, Tlemcen-Parc national de Tlemcen, Tizi-n-Hafir (1,260 m): HAL 107954: HE649610, HE649706, HE649519. G. chrysantha Schult. & Schult.f.: CHRY: Italy, Sicily, Ficuzza (600 m)—locus classicus: CLU 9237: AM283110, AM409353, AM287284. G. cossoniana Pascher: COS1: Morocco, Marrakech-Ait Barka (1000 m): HAL 107915: HE649593, HE649689, HE649502; COS2: Morocco, Meknes-Ifrane (1650 m): HAL 107914: HE649594, HE649690, HE649503; COS3: Spain, Malaga, Ronda (1,200 m): HAL 107851: HE649595, HE649691, HE649504. G. dubia A.Terracc.: DUB1*: Turkey, SW Türkei, Ak dag, Gömbe (1750 m): HAL 108496: HE649664, HE649761, -; DUB2*: Turkey, Central Taurus (Isauria), Akseki district (900 m): PI s.n.: HE649665, HE649762, -; DUB3*: Turkey, Western Taurus (Lycia), Thermessos National Park (1,024 m): PI s.n.: HE649666, HE649763, HE649571; DUB4*: Turkey, SW-Turkey, S-Babadag (1,200 m): HAL 108498: HE649667, HE649764, HE649572; DUB5*: Greece, Crete Hania- Omalos: secteur de Kallergi (1,300–1,600 m): HAL 107865: HE649668, HE649765, HE649573. G. durieui Parl.: DUR1: Morocco, Oujda-Taforalt, col de la S403 au N du village (500 m): HAL 107863: HE649615, HE649711, HE649523; DUR2: Spain, Granada, Velez-de-Benaudalla, colline dominant le village (200 m): HAL 107864: HE649616, HE649712, HE649524; DUR3: Spain, Baleares, Mallorca, Llucmajor: entre Son Granada Nou, Puigderros d’Alt et Puigderros de Baix (120 m): HAL 108492: HE649617, HE649713, HE649525; DUR4: Algeria, Sidi-Bel-Abbes-Sidi-bel-Abbès: HAL 108493: HE649618, HE649714, HE649526. G. elliptica (A.Terrac.) Prain: EL1*: Spain, Grazalema, à l’est du Puerto de las Palomas (1,250 m): HAL 107861: HE649619, HE649715, HE649527; EL2*: Spain, Jubrique, au N du Puerto de Penas Blancas (1,000 m): HAL 107860: HE649620, HE649716, HE649528. G. foliosa (C.Presl) Schult. & Schult.f.: FOL1: Algeria, Bouira-Tikjda (1,540 m): HAL 107852: HE649621, HE649717, HE649529; FOL2: Italy, Sardinia, Oliena, montée au Sopramonte (900 m): HAL 107854: HE649622, HE649718, HE649530; FOL3: Italy, Sardinia, Oliena, col Corrasi (1,300 m): HAL 107853: HE649623, HE649719, HE649531; FOL4: Italy, Sardinia, Orani (800 m): HAL 104326: AM903066, AM903063, -; FOL5: Italy, Sicily, Madonie (1,600 m): CLU 12691: AM265603, AM282993, AM409346; FOL6: Italy, Sicily, Petralia Sottana (900 m): HAL 107855: HE649624, HE649720, HE649532. G. fragifera (Vill.) Ehr.Bayer & G.López (= G. liotardii (Sternberg) Schult. & Schult.f.): FRA1: France, Alpes-Maritimes, Saint-Dalmas-le-Selvage (1,950 m): HAL 104325: FN868223, FN868197, FN868165; FRA2: Italy, Calabria, Verbicaro-Orsomarso mountains (1,263 m): CLU 12693: AM283103, AM282994, AM422468; FRA3: France: S France, versante meridionale di Col de la Cayolle (2000 m): PI s.n.: FN868224, FN868201, FN868166; FRA4: Italy, Piemonte, Valle di Bellino (Cuneo), sopra Rif. Melezè: PI s.n.: FN868225, FN868202, FN868167; FRA5: Italy, Sicily, Madonie (1,650 m): CLU 12692: AM283102, AM282995, AM287285; FRA6: Bulgaria, Pirin: HAL 070407: AJ890368, AJ973158, -; FRA7: China, Xinjiang Thianchi Lake: HAL 107898: FN868226, FN868198, -; FRA8: Kazakhstan: HAL 101796: AM161467, AM238521, -; FRA9: Switzerland, Canton Graubuenden, Jufner Alp: ZT-10726: AJ890375, AM238531, -; FRA10: Ukraine, Crimea: HAL 101797: AM161466, AM238522, -. G. glacialis K.Koch: GLA1: Turkey, Rize district Ovitdagi Gecidi (2,800 m): HAL 101647: AM287281, AM265586, AM265535; GLA2: Turkey, Zigana Pass, Prov. Trabzon: HAL 107881: FN868234, FN868206, -. G. granatellii (Parl.) Parl.: GRA1: France, Corse, Tolla, col de Mercujo (720 m): HAL 107957: HE649625, HE649721, HE649533; GRA2: France, Herault, Lacaunette (350 m): HAL 107856: HE649626, HE649722, HE649534; GRA3: Italy, Calabria, Sila (600 m): CLU 9266: AM265598, AM282988, AM409344; GRA4: Italy, Tuscany, Isola del Giglio (390 m): PI s.n.: HE649627, HE649723, HE649535; GRA5: Italy, Tuscany, Elba Island (600 m): PI s.n.: HE649628, HE649724, HE649536; GRA6: Italy, Apulia, Murge, S. Paolo, Taranto (300 m): CLU 18184: HE649629, HE649725, HE649537; GRA7: Italy, Apulia, Murge, S. Simone, Taranto (250 m): CLU 18176: HE649630, HE649726, HE649538; GRA8: Italy, Sardinia, Orani (800 m): HAL 104330: AM903067, AM903058, -; GRA9: Italy, Sardinia, Sassari, Tempio Pausania (800 m): HAL 104329: HE649631, HE649727, HE649539; GRA10: Italy, Sicily, Iblei, Monte Lauro (950 m): CLU 9267: AM265599, AM282989, AM409343; GRA11: Tunisie, Tabarka, arrière-plage de Barkoukech (30 m): HAL 107961: HE649632, HE649728, HE649540. G. heldreichii (A.Terracc.) Stroh: HEL1: Greece, Attiki, Agia Triada (1,300 m): HAL 107857: HE649633, HE649729, HE649541; HEL2: Greece, Attiki-Agia Triada (1,300 m): HAL 107874: HE649634, HE649730, HE649542; HEL3: Greece, Crete Hania-Omalos, plaine entre le village et le col de Xyloskalo (1,100 m): HAL 107873: HE649635, HE649731, HE649543. G. lacaitae A.Terracc.: LAC1: France, Gignac, les Piélettes c. 10 m, friche au bord de l’autoroute: HAL 075509: HE649636, HE649732, HE649544; LAC2: France, Herault: HAL 101837: AM265515, AM265592, AM409333; LAC3: France, Réauville, plateau de St-Pancrace (200 m): HAL 107909: HE649637, HE649733, HE649545; LAC4: Italy, Abruzzo, Gran Sasso (1,100 m): CLU 14924: AM265597, AM282990, AM409342; LAC5: Italy, Sicily, Caltagirone aI’ene de la ville pres du lieu dit Ogliastro (300 m): HAL 107910: HE649638, HE649734, HE649546; LAC6: Spain, Malaga, Ronda, Puerto del Viento (1,150 m): HAL 105936: HE649639, HE649735, HE649547; LAC7: Spain, Malaga, Ronda, Puerto del Viento (1150 m): HAL 071229: HE649640, HE649736, HE649548. G. lojaconoi Peruzzi: LOJ1: Italy, Calabria, San Marco Argentano (180 m): CLU 9256: AM283106, AM282997, AM287272; LOJ2: Italy, Apulia, Monte Sant’Angelo, Foggia, au-dessus du village sur la route du Gargano (800 m): HAL 107908: HE649641, HE649737, HE649549; LOJ3: Italy, Sicily, Iblei, Monte Lauro (950 m): CLU 9253: AM283107, AM282998, AM422464. G. luberonensis J.-M.Tison: LUB1*: France, Ardiche, Berrias-et-Casteljau (170 m): HAL 107870: HE649642, HE649738, HE649550; LUB2*: France, Gard, Sommieres (150 m): HAL 107871: HE649643, HE649739, HE649551; LUB3*: France, Vaucluse, Cheval-Blanc (250 m)—locus classicus: HAL 105944: FM200221, HE649740, -; LUB4*: France, Taillades, pied du Petit Luberon, vallon de la Combe (180 m): HAL 107907: HE649644, HE649741, HE649552; LUB5*: France, Berrias-et-Casteljau, plateau du Gras de la Rouveyrolle (170 m): HAL 107904: HE649645, HE649742, HE649553; LUB6*: France, Robion, au S.-E. de la bergerie du Colombier (550 m): HAL 107906: HE649646, HE649743, HE649554; LUB7*: France, Sommières, plateau de Fontbouisse (150 m): HAL 107905: HE649647, HE649744, HE649555; LUB8*: Italy, Abruzzo, Gran Sasso (1,100 m): CLU 14926: AM283105, AM283000, AM422467; LUB9*: Italy, Latium, M. Tancia (1,100 m): CLU 20581: AM903068, AM903062, AM422463. G. cf. luberonensis LUB10*: France, Bouches-de-Rhone, Auriol (600 m): HAL 107859: HE649648, HE649745, HE649556. G. lusitanica A.Terracc.: LUS1*: Spain, Grazalema, à l’est du Puerto de las Palomas (1,250 m): HAL 107887: HE649649, HE649746, HE649557; LUS2*: Spain, Granada, Loja, N321 au pied de la montagne de Los Infiernos (900 m): HAL 108500: HE649650, HE649747, HE649558; LUS3*: Spain, Malaga, Ronda, versant ouest du Puerto del Viento (1,100 m): HAL 107911: HE649651, HE649748, HE649559. G. mauritanica Durieu: MAU1: Algerine, Oran, St. Eugene: HAL 107901: HE649652, HE649749, -; MAU2: Spain, Baleares, Mallorca, Llucmajor (120 m): HAL 107903: HE649653, HE649750, HE649560; MAU3 Spain, Baleares, Mallorca, Llucmajor (120 m): HAL 107900: HE649654, HE649751, HE649561. G. microfistulosa Levichev: MICRO*: Ukraine, Crimea: HAL 101728: AM265517, AM265589, AM409332. G. moniliformis J.-M. Tison: MONIL*: Morocco, Marrakech-Oukaimeden, à la station 2,700 m: HAL 107866: HE649655, HE649752, HE649562. G. nevadensis Boiss.: NEV1: Spain, Granada, Monachil (1,900 m)—locus classicus: HAL 107888: HE649656, HE649753, HE649563; NEV2: Spain, Granada, Monachil (1,900 m)—locus classicus: HAL 107889 (DNA1): HE649657, HE649754, HE649564; NEV3: Spain, Granada, Monachil (1,900 m)—locus classicus: HAL 107889 (DNA2): HE649658, HE649755, HE649565. G. omalensis J.-M.Tison: OM1: Greece, Crete Hania, Omalos, plaine entre le village et le col de Xyloskalo (1,100 m): HAL 107877: HE649659, HE649756, HE649566; OM2: Greece, Crete Hania, Omalos Plateau: HAL 108490: HE649660, HE649757, HE649567. G. peduncularis (J.Presl & C.Presl) Pascher: PED1: Greece, Fokida- Lilea, contreforts du Mont Parnasse (800 m): HAL 107885: HE649661, HE649758, HE649568; PED2: Italy, Apulia, Murge, Taranto (252 m): CLU 18163-18165: AM409357, AM903056, AM903050; PED3: Greece, East Crete, Ori Thriptis, near Orino: HAL 108499: HE649662, HE649759, HE649569. G. peruzzii J.-M.Tison: PERU1*: Italy, Calabria, Verbicaro-Orsomarso mountains (1,260 m): CLU 12688: AM932485, AM932484, AM931940; PERU2*: Italy, Basilicata, Pollino Massif (1,300 m): CLU 12685: HE649608, HE649704, HE649517; PERU3*: Italy, Calabria, Pollino Massif (1,000 m): CLU 9236: HE649609, HE649705, HE649518. G. polidorii J.-M. Tison: POL1*: France, Corse, Sorio, au niveau du col entre les Monte Grimaesta et Astu (1,450 m): HAL 107416: FN868238, FN868212, FN868186; POL2*: France, Alpes-Maritimes, Saint-Dalmas-le-Selvage (1,950 m): HAL 107417: FN868237, FN868211, FN868187; POL3*: Italy, Calabria, Verbicaro-Orsomarso mountains (1,263 m): CLU 12700: AM283104, AM282999, AM903053. G. polymorpha Boiss.: POLY1: Spain, Granada—La Calahorra (1,250 m): HAL 107913: HE649669, HE649766, HE649574; POLY2: Spain, Granada –Padul, contreforts ouest de la Sierra del Manar (1,000 m): HAL 107912: HE649670, HE649767, HE649575. G. pseudopeduncularis J.-M.Tison: PSEUD*: Greece, Attiki—Agia Triada, crête du Mont Parnes (1,300 m): HAL 107886: HE649663, HE649760, HE649570. G. ramulosa A.Terracc.: RAM1: Italy, Abruzzo, Altopiano delle Rocche (1,270 m): APP 20580: AM409360, AM409355, AM422462; RAM2: Italy, Sardinia, Supramonte (1,350 m): HAL 104332: AM903064, AM903054, AM903048; RAM3: Spain, Granada, Monachil (1,900 m): HAL 107868: HE649611, HE649707, HE649520; RAM4: Turkey, Central Taurus (Isauria), Ibradi district, Gembos pasture (1,300–1,400 m): PI s.n. (DNA1): HE649612, HE649708, HE649521; RAM5: Turkey, Central Taurus (Isauria), Ibradi district, Gembos pasture (1,300–1,400 m): PI s.n. (DNA2): HE649613, HE649709, -; RAM6: Turkey, SW, Korkuteli-Antalya (1,200 m): HAL 108497: HE649614, HE649710, HE649522. G. sicula Lojac.: SIC: Italy, Ficuzza, Palermo, sommet du Monte Cucco (1,100 m): HAL 107884: HE649671, HE649768, HE649576. G. soleirolii F.W.Schultz: SOL1: Italy, Sardinia, Nuoro—Fonni, montée au Bruncu Spinu (1,500–1,600 m): HAL 107955: HE649672, HE649769, HE649577; SOL2: Italy, Sardinia, M. Limbara (1,300 m): CLU 9257: AM903069, AM409352, -; SOL3: Italy, Sardinia, M. Bruncu Spina (1,500 m): HAL 104327: AM903070, AM903060, -; SOL4: Portugal, Beira Baixa, Casal-da- Serra (700 m): HAL 105938: FM200220, HE649770, -. G. subtrigona J.-M.Tison: SU1*: Morocco, Meknes—Timhadite, Tizi-n-Tretten (1,900 m): HAL 107414: HE649673, HE649771, HE649578; SU2*: Morocco, Ouarzazate—Aguelmouss: près du Tizi-n-Tichka (2,300 m): HAL 107412: HE649674, HE649772, HE649579; SU3*: Spain, Cazorla, Puerto de las Palomas (1,300 m): HAL 107415 (DNA1): HE649675, HE649773, HE649580; SU4*: Spain, Cazorla, Puerto de las Palomas (1,300 m): HAL 107415 (DNA2): HE649676, HE649774, HE649581; SU5*: Spain, Robledo, col de la N322 à la sortie W de la ville (1,000 m): HAL 107409 (DNA1): HE649677, HE649775, HE649582; SU6*: Spain, Robledo, col de la N322 à la sortie W de la ville (1,000 m): HAL 107409 (DNA2): HE649678, HE649776, HE649583; SU7*: Spain, Priego-de-Cordoba, plateau de Navazuelo (800 m): HAL 107413 (DNA1): HE649679, HE649777, HE649584; SU8*: Spain, Priego-de-Cordoba, plateau de Navazuelo (800 m): HAL 107413 (DNA2): HE649680, HE649778, HE649585; SU9*: Spain, Malaga, Ronda, à l’ouest du Puerto del Viento (1,200 m): HAL 107411 (DNA1): HE649681, HE649779, HE649586; SU10*: Spain, Malaga, Ronda, à l’ouest du Puerto del Viento (1,200 m): HAL 107411 (DNA2): HE649682, HE649780, HE649587; SU11*: Spain, Malaga, Ronda, à l’ouest du Puerto del Viento (1,200 m): HAL 107411 (DNA3): HE649683, HE649781, HE649588; SU12*: Spain, Alcolea, voie express NII à 1,5 km à l’est du Puerto de Alcolea (1,100 m): HAL 107410: HE649684, HE649782, HE649589. G. tenera Pascher: TEN: Kyrgyzstan (1,100 m): HAL 101843: AM238535, AM238527, AM422460. G. villosa (M.Bieb.) Sweet: VIL1: Austria, Niederoesterreich, Wien: Türkenschanzpark (300 m): HAL 107418: FN868246, FN868220, FN868188; VIL2: France, Corse, Sorio: au niveau du col entre les Monte Grimaesta et Astu (1,450 m): HAL 107419: FN868244, FN868218, FN868190; VIL3: Bulgaria, Village Sushevo (230 m): PI s.n.: FN868239, FN868214, FN868189; VIL4: Germany, Saxony-Anhalt: -: AJ419163, AJ416373, AJ427545; VIL5: Greece, Epiros, Monts Timfi, parc national du Vikos-Aoos: HAL 107420: FN868243, FN868217, FN868192; VIL6: France: Alpes-Maritimes, Saint-Dalmas-le-Selvage (1,500 m): HAL 107422: FN868242, FN868213, -; VIL7: France, Optevoz, cimetière (300 m): HAL 107421: FN868245, FN868219, FN868191; VIL8: Italy, Abruzzo, Barisciano (800 m): CLU 14928: AM265605, AM282991, AM287283; VIL9: Italy, Calabria, Verbicaro-Orsomarso mountains (1,000 m): CLU 15219: AM265604, AM282992, AM409345; VIL10: Italy, Piemonte, Valle Stura di Demonte (1,600 m): PI s.n.: FN868240, FN868215, FN868193; VIL11: Turkey, Western Taurus (Lycia), Elmali district, Cedrus Research Forest (1,600 m): PI s.n.: HE649685, HE649783, HE649590; VIL12: Turkey, Central Taurus (Isauria), Ibradi district, Gembos pasture (1,300–1,400 m): PI s.n.: HE649686, HE649784, HE649591; VIL13: Turkey, Western Taurus (Lycia), Thermessos National Park (1001 m): PI s.n.: HE649687, HE649785, HE649592.

Outgroups ( Gagea ): Gagea bulbifera (Pall.) Salisb.: -: Russia: HAL 101840, LE 2/04DNALevichev: AJ969119, AM049260, AM162669. G. circumplexa Vved.: -: Uzbekistan: HAL 101795, LE 30/04DNALevichev: AJ969122, AJ973172, AM265529. G. gageoides (Zucc.) Vved.: -: Kazakhstan: HAL 101792, LE 41/04DNALevichev: AM084905, AM161462, AM162673. G. graeca (L.) Irmisch.: -: Greece: B 100073942: AM779096, AM779097, AJ810088. G. minima (L.) Ker Gawl.: MIN: Italy, Calabria, Pollino Massif, Manfriana (1850 m): CLU 12698: AM283109, AM282996, AM287273. G. pauciflora Turcz. ex Ledeb.: -: Russia: HAL 103857, LE 1/04DNALevichev: AM161468, AM287266, AM493952. G. pratensis (Pers.) Dumort.: -: Italy: CLU 12703: AM265607, AM903059, AM903047. G. reticulata (Pall.) Schult. & Schult.f.: -: Israel: Z 34650: AJ890371, AJ973161, AM087954. G. serotina (L.) Ker Gawl.: -: Kazakhstan: HAL 101789, LE 45a/04DNALevichev.: AJ890376, AM238530, AM087956. G. spathacea (Hayne) Salisb.: SPAT: Italy, Emilia-Romagna, Serramazzoni (758 m): CLU 17518: AM283108, AM409347, AM422465. G. stipitata Merckl. ex Bunge: -: Iran: HAL 101828, LE 49/04DNALevichev: AM265519, AM265594, AM409336. G. triflora (Ledeb.) Schult. & Schult.f.:-: Russia: HAL 101788, LE 46/04DNA Levichev: AJ890377, AM049261, AM162674. Outgroups (Liliaceae): Tulipa cretica Boiss. & Heldr.: -: Greece, Crete: HAL 099934: AJ810118, AM049257, AM180461. Erythronium californicum Purdy: -: -: -, -, AF485292#. Erythronium japonicum Decne: -: HAL 112567: HE649688, HE649786, -. Lilium candidum L.:-: -: AJ430416, AJ431692, AB020464#. Fritillaria latifolia Willd.: -: -, -, AM292420#.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tison, JM., Peterson, A., Harpke, D. et al. Reticulate evolution of the critical Mediterranean Gagea sect. Didymobulbos (Liliaceae) and its taxonomic implications. Plant Syst Evol 299, 413–438 (2013). https://doi.org/10.1007/s00606-012-0731-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-012-0731-4

Keywords

Navigation