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Hybridization drives speciation in Gagea (Liliaceae)

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Abstract

Hybridization seems to play an important role in speciation of Gagea Salisb., a genus which is characterised by polyploid taxa lines and in which diploids (2= 24) appear only to be common in basal sections. Hybrid detection was applied utilising direct and cloning nrDNA ITS data (ITS1, 5.8S rDNA, ITS2) combined with neighbour and ribotype networks and discussed in connection with previously published cpDNA, morphological and karyological data of the authors. We have evidence of the hybrid origin of taxa within the section Gagea (G. pomeranica, G. megapolitana) and the monophyletic clade of sections Didymobulbos and Fistulosae (G. microfistulosa, G. polidorii, G. cf. bohemica). Morphologically and karyologically differentiated Gagea megapolitana and G. pomeranica, adapted to synanthropic habitats, represent both hybrids of G. pratensis × G. lutea. Gagea microfistulosa represents a hybrid of G. villosa × G. fragifera; Gagea polidorii could represent the reverse hybrid. G. glacialis is also closely related to the latter complex.

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References

  • Abbott RJ, Lowe AJ (2004) Origins establishment and evolution of two new polyploidy species of Senecio in British Isles. Biol J Linnean Soc 82:467–474

    Article  Google Scholar 

  • Ainouche ML, Baumel A, Salmon A, Yannic G (2004) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172

    Article  CAS  Google Scholar 

  • Albarouki E, Peterson A (2007) Molecular and morphological characterization of Crataegus L. species (Rosaceae) in southern Syria. Bot J Linnean Soc 153:255–263

    Article  Google Scholar 

  • Allen GA, Soltis DE, Soltis PS (2003) Phylogeny and biogeography of Erythronium (Liliaceae) inferred from chloroplast matK and nuclear rDNA ITS sequences. Syst Bot 28:512–523

    Google Scholar 

  • Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434

    Article  PubMed  CAS  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Boissier E (1882) Gagea. Flora Orientalis. Geneve et Basiliae 5:203–211

    Google Scholar 

  • Booy G, Van der Schoot J, Vosman B (2000) Heterogeneity of the internal transcribed spacer 1 (ITS1) in Tulipa (Liliaceae). Plant Syst Evol 225:29–41

    Article  CAS  Google Scholar 

  • Caparelli KF, Peruzzi L, Cesca G (2006) A comparative analysis of embryo-sac development in three closely-related Gagea Salisb. species (Liliaceae), with some consideration on their reproductive strategies. Plant Biosyst 140:115–122

    Article  Google Scholar 

  • Chen ZJ, Ha M, Soltis D (2007) Polyploidy: genome obesity and its consequences. New Phytol 174:717–720

    Article  PubMed  CAS  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, Levichev IG (1987) Chromosome numbers of species of the genus Gagea from Middle Asia. Bot J (Leningr) 72:1271–1272

    Google Scholar 

  • Eickbush TH, Eickbush DG (2007) Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    Article  PubMed  CAS  Google Scholar 

  • Elder JF Jr, Turner BJ (1995) Concerted evolution of repetitive DNA sequences in eukaryotes. Q Rev Biol 70:297–320

    Article  PubMed  CAS  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 

  • Grimm GW, Denk T (2008) ITS evolution in Platanus (Platanaceae): homoeologues, pseudogenes and ancient hybridization. Ann Bot 101:403–419

    Article  PubMed  CAS  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 (2008) 5.8S motifs for the identification of pseudogenic ITS regions. Botany 86:300–305

    Article  CAS  Google Scholar 

  • Hegarty MJ, Hiscock SJ (2005) Hybrid speciation in plants: new insights from molecular studies. New Phytol 165:411–423

    Article  PubMed  CAS  Google Scholar 

  • Henker H (2005) Die Goldsterne von Mecklenburg-Vorpommern unter besonderer Berücksichtigung kritischer und neuer Sippen. Botanischer Rundbrief für Mecklenburg-Vorpommern 39:5–88

    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 

  • Huson DH, Kloepper TH (2005) Computing networks from binary sequences. Bioinformatics 21:159–165

    Article  Google Scholar 

  • Ikinci N, Oberprieler C, Güner A (2006) On the origin of European lilies: phylogenetic analysis of Lilium section Liriotypus (Liliaceae) using sequences of the nuclear ribosomal transcribed spacers. Willdenowia 36:647–656

    Article  Google Scholar 

  • Leitch IJ, Beaulieu JM, Cheung K, Hanson L, Lysak MA, Fay MF (2007) Punctuated genome size evolution in Liliaceae. J Evol Biol 20:2296–2308

    Article  PubMed  CAS  Google Scholar 

  • Levichev IG (1990) On age variation and hybridization of some representatives of Gagea (Liliaceae). Bot J (Leningr) 75:658–667

    Google Scholar 

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

    Google Scholar 

  • Levichev IG (1999b) Zur Morphologie in der Gattung Gagea Salisb. (Liliaceae). I. Die unterirdischen Organe. Flora 194:379–392

    Google Scholar 

  • Levichev IG (2001) New species of the genus Gagea Salisb. (Liliaceae) from western districts of Asia. Turczaninowia 4:5–35

    Google Scholar 

  • Levichev IG (2005) New taxa of the genus Gagea (Liliaceae) in the flora of the Caucasus. Bot J (St. Petersburg) 90:1580–1592

    Google Scholar 

  • Levichev IG (2006a) A review of the Gagea (Liliaceae) species in the flora of Caucasus. Bot J (St. Petersburg) 91:917–951

    Google Scholar 

  • Levichev IG (2006b) Four new species of the genus Gagea Salisb. (Liliaceae) from Western Himalayas and the adjoining regions. Pakistan J Bot 38:47–54

    Google Scholar 

  • Levichev IG (2008a) System of genus Gagea (Liliaceae) from positions of the neotenical divergence. Turczaninowia 11 (in press)

  • Levichev IG (2008b) New species of genus Gagea Salisb. (Liliaceae) from the Crimean yaila. Novitates systematicae plantarum vascularium, Moscow, St. Petersburg. T. 40 (in press)

  • Lim KY, Matyasek R, Kovarik A, Leitch A (2007) Parental origin and genome evolution in the allopolyploid Iris versicolor. Ann Botany 100:219–224

    Article  CAS  Google Scholar 

  • Linder CR, Rieseberg H (2004) Reconstructing patterns of reticulate evolution in plants. Am J Bot 91:1700–1708

    Article  PubMed  Google Scholar 

  • Mahelka V, Fehrer J, Krahulec F, Jarolímová V (2007) Recent natural hybridization between two allopolyploid wheatgrasses (Elytrigia, Poaceae): Ecological and evolutionary implications. Ann Botany 100:249–260

    Article  CAS  Google Scholar 

  • McBreen K, Lockhart PJ (2006) Reconstruction reticulate evolutionary histories of plants. Trends Plant Sci 11:398–404

    Article  PubMed  CAS  Google Scholar 

  • McDade LA (1992) Hybrids and phylogenetic systematics II. The impact of hybrids on cladistic analysis. Evolution 46:1329–1346

    Article  Google Scholar 

  • Nishikawa T, Okazaki K, Uchino T, Arakawa K, Nagamine T (1999) A molecular phylogeny of Lilium in the internal transcribed spacer region of nuclear ribosomal DNA. J Mol Evol 49:238–249

    Article  PubMed  CAS  Google Scholar 

  • Okuyama Y, Fujii N, Wakabayashi M, Kawakita A, Ito M, Watanabe M, Murakami N, Kato M (2005) Nonuniform converted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae). Mol Biol Evol 22:285–296

    Article  PubMed  CAS  Google Scholar 

  • Paun O, Fay MF, Soltis DE, Chase MW (2007) Genetic and epigenetic alterations after hybridization and genome doubling. Taxon 56:649–656

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Peruzzi L (2008b) Hybridity as a main evolutionary force in the genus Gagea Salisb. (Liliaceae). Plant Biosyst 142:179–184

    Google Scholar 

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

    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, Peterson A, Tison J-M, Peterson J (2007) Phylogenetic Relationships of Gagea Salisb. (Liliaceae) in Italy, inferred from molecular and morphological matrixes. XII Optima Meeting, Pisa, Italy, 10–16 September 2007. p. 118

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

    Google Scholar 

  • Peruzzi L, Peterson A, Tison J-M, Peterson J (2008b) Phylogenetic relationships of Gagea Salisb. (Liliaceae) in Italy, inferred from molecular and morphological data matrixes. Pl Syst Evol 276:219–234. doi:10.1007/s00606-008-0081-4

    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. Plant Syst Evol 245:145–162

    Article  CAS  Google Scholar 

  • Peterson A, Levichev IG, Peterson A (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 

  • Rieseberg LH, Willis JH (2007) Plant Speciation. Science 317:910–914

    Article  PubMed  CAS  Google Scholar 

  • Rix EM (1984) Gagea Salisb. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands. Edinburgh, pp. 312–327

  • Ronsted N, Law S, Thornton H, Fay MF, Chase MW (2005) Molecular phylogenetic evidence for the monophyly of Fritillaria and Lilium (Liliaceae; Liliales) and the infrageneric classification of Fritillaria. Mol Phylogenet Evol 35:509–527

    Article  PubMed  CAS  Google Scholar 

  • Saito Y, Kokubugata G, Möller M (2007) Molecular evidence for a natural hybrid origin of Doellingeria x sekimotoi (Astaraceae) using ITS and matK sequences. Int J Plant Sci 168:469–476

    Article  CAS  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  CAS  Google Scholar 

  • Schnare MN, Damberger SH, Gray MW, Gutell RR (1996) Comprehensive comparison of structural characteristics in eukaryotic cytoplasmic large subunit (23 S-like) ribosomal RNA. J Mol Biol 256:701–719

    Article  PubMed  CAS  Google Scholar 

  • Schwarzbach AE, Rieseberg LH (2002) Likely multiple origin of a diploid hybrid sunflower species. Mol Ecol 11:1703–1715

    Article  PubMed  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Tate JA (2004a) Advances in the study of polyploidy since plant speciation. New Phytol 161:173–191

    Article  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E (2004b) Recent and recurrent polyploidy in Tragopogon (Asteraceaee). Cytogenic, genomic, and genetic comparisons. Biol J Linnean Soc 82:485–501

    Article  Google Scholar 

  • Suárez-Santiago VN, Salinas MJ, Romero-García AT, Garrido-Ramos MA, de la Herrán R, Ruiz-Rejón C, Ruiz-Rejón M, Blanca G (2007) Polyploidy, the major speciation mechanism in Muscari subgenus Botryanthus in the Iberian Peninsula. Taxon 56:1171–1184

    Google Scholar 

  • Tison JM (1998) Note complementaire sur quelques Gagea francais. Le Monde des Plantes. 462:7–8

    Google Scholar 

  • Tison JM (2004) Gagea polidorii J.M. Tison, an unrecognised species from South western Alps and Apennines. Acta Botanica Gallica 151:319–326

    Google Scholar 

  • Volkov RA, Komarova NY, Hemleben V (2007) Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodivers 5:261–276

    Article  Google Scholar 

  • Vriesendorp B, Bakker FT (2005) Reconstruction pattern of reticulate evolution in angiosperms: what can we do? Taxon 54:593–604

    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 

  • Wissemann V (2007) Plant evolution by means of hybridization. Syst Biodivers 5:243–253

    Article  Google Scholar 

  • Zarrei M, Zarre S, Wilkin P, Rix M (2007) Systematic revision of the genus Gagea Salisb. (Liliaceae) in Iran. Bot J Linnean Soc 154:559–588

    Article  Google Scholar 

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Peterson, A., Harpke, D., Peruzzi, L. et al. Hybridization drives speciation in Gagea (Liliaceae). Plant Syst Evol 278, 133–148 (2009). https://doi.org/10.1007/s00606-008-0102-3

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