Abstract
Rhinanthoid Orobanchaceae form a monophyletic lineage that include the hemiparasitic genera Euphrasia, Melampyrum, Tozzia, Bartsia, Nothobartsia, Odontites (s.l.), Rhinanthus, Rhynchocorys, Parentucellia, Hedbergia and holoparasitic Lathraea. In this study, we aimed to reconstruct the phylogeny, evolution of life-history traits (life cycle and seed size) and explain the extant biogeographical patterns in this group. For phylogenetic reconstruction, we used molecular data obtained by sequencing the nuclear ITS region and the chloroplast trnT-trnL intergenic spacer and matK + trnK regions. The genus Melampyrum was found to occupy the sister position to the rest of the group. The other genera were assembled in the sister Rhinanthus-Rhynchocorys-Lathraea and Bartsia-Euphrasia-Odontites subclades. The reconstruction of life-cycle evolution yielded ambiguous results suggesting nonetheless a substantially higher likelihood of perenniality compared to annuality in most ancestor lineages. Seed size varied across two orders of magnitude (average weight per seed: 0.02–7.22 mg) and tended to decrease in the Bartsia-Euphrasia-Odontites subclade compared to the rest of the group. Seed-size evolution was correlated with life-history evolution in the group if the generally small-seeded Bartsia-Euphrasia-Odontites subclade is excluded. We formulated hypotheses relating the extant biogeographical affinities of individual genera to the geological history of the Euro-Caucasian diversity center of the group. Notable dispersal events in Euphrasia and Bartsia were hypothesized to be allowed or at least facilitated by a specific combination of the life-history traits.
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References
Albaladejo RG, Fuertes Aguilar J, Aparicio A, Nieto Feliner G (2005) Contrasting nuclear-plastidial phylogenetic patterns in the recently diverged Iberian Phlomis crinita and P. lychnitis lineages (Lamiaceae). Taxon 54:987–998
Andreasen K, Baldwin BG (2001) Unequal evolutionary rates between annual and perennial lineages of checker mallows (Sidalcea, Malvaceae): Evidence from 18S–26S rDNA internal and external transcribed spacers. Molec Biol Evol 18:936–944
Bennett JR, Mathews S (2006) Phylogeny of the parasitic plant family Orobanchaceae inferred from phytochrome A. Amer J Bot 93:1039–1051
Bolliger M, Molau U (1992) Nothobartsia, a new genus of Scrophulariaceae from southwest Europe. Pl Syst Evol 179:59–71
Bolliger M, Wick L (1990) The pollen morphology of Odontites (Scrophulariaceae) and its taxonomic significance. Pl Syst Evol 173:159–178
Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, van der Bank M, Chase MW, Hodkinson TR (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): Progress towards complete tribal and generic level sampling. Molec Phylogen Evol 47:488–505
Bullock JM, Moy IL, Coulson SJ, Clarke RT (2003) Habitat-specific dispersal: environmental effects on the mechanisms and patterns of seed movement in a grassland herb Rhinanthus minor. Ecography 26:692–704
Castroviejo S, Benedí C, Rico E, Güelmes J, Herrero A (2009) Flora Iberica, 13. Real Jardín Botánico, Madrid
Conti E, Soltis DE, Hardig TM, Schneider J (1999) Phylogenetic relationships of the silver saxifrages (Saxifraga, Sect. Ligulatae Haworth): Implications for the evolution of substrate specificity, life histories, and biogeography. Molec Phylogen Evol 13:536–555
Coomes DA, Grubb PJ (2003) Colonization, tolerance, competition and seed-size variation within functional groups. Trends Ecol Evol 18:283–291
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchman N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook for standardised and easy measurement of plant functional traits worldwide. Austral J Bot 51:335–380
Cronn RC, Small RL, Haselkorn T, Wendel JF (2002) Rapid diversification of the cotton genus (Gossypium: Malvaceae) revealed by analysis of sixteen nuclear and chloroplast genes. Amer J Bot 89:707–725
Datson PM, Murray BG, Steiner KE (2008) Climate and the evolution of annual/perennial life-hisotries in Nemesia (Scrophulariaceae). Pl Syst Evol 270: 39–57
Davis PH (1978) Flora of Turkey and the East Aegean Islands, 6. Edinburgh University Press, Edinburgh
Dezes P, Schmid SM, Ziegler PA (2004) Evolution of the European Cenozoic rift system: interaction of the Alpine and Pyrenean orogens with their foreland lithosphere. Tectonophysics 389:1–33
Eriksson O, Jakobsson A (1998) Abundance, distribution and life histories of grassland plants: a comparative study of 81 species. J Ecol 86: 922–933
Felsenstein J (1985) Phylogenies and the comparative method. Amer Naturalist 125:1–15
Fiz O, Valcárcel V, Vargas P (2002): Phylogenetic position of Mediterranean Astereae and character evolution of daisies (Bellis, Asteraceae) inferred from nrDNA ITS sequences. Molec Phylogen Evol 25:157–171
Fujii N, Ueda K, Watano Y, Shimizu T (1997) Intraspecific sequence variation of chloroplast DNA in Pedicularis chamissonis Steven (Scrophulariaceae) and geographic structuring of Japanese “alpine” plants. J Pl Res 110: 195–207
Gabrielian EC (1987) Scrophulariaceae. In Takhtajan AL (ed) Flora Armenii 8. Izdatel’stvo Akademii nauk Armyanskoi SSR, Erevan, pp 186–359
Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Liu AZ, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, Ross-Fraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281
Gussarova G, Popp M, Vitek E, Brochmann C (2008) Molecular phylogeny and biogeography of the bipolar Euphrasia (Orobanchaceae): Recent radiations in an old genus. Molec Phylogen Evol 48:444–460
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
Hedberg O (1957) Afroalpine vascular plants. a taxonomic revision. A.-B. Lundequistska Bokhandeln,Uppsala
Heide-Jørgensen HS (2008) Parasitic flowering plants. Koninklijke Brill NV, Leiden
Irving LJ, Cameron DD (2009) You are what you eat: interactions between root parasitic plants and their hosts. Advances Bot Res 50:87–138
Jacobsson A, Eriksson O (2000) A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88:494–502
Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156
Katoh K, Kuma K, Toh H, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066
Kubat R, Weber HC (1987) Zur Biologie von Rhynchocorys elephas (L.) Griseb. (Scrophulariaceae). Beitr Biol Pflanzen 62:239–250
Lewis PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50:913–925
Liu K, Eastwood RJ, Flynn S, Turner RM, Stuppy WH (2008): Seed Information Database (release 7.1). Kew. Available at: http://www.kew.org/data/sid
Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis, version 2.6. Available at: http://mesquiteproject.org
Meusel H, Jäger E, Rauschert S, Weinert E (1978) Vergleichende Chorologie der zentraleuropäischen Flora, 2. VEB Gustav Fischer Verlag, Jena
Molau U (1988) Hedbergia, a new genus of Scrophulariaceae from Africa. Nordic J Bot 8:193–195
Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M (2005) A brief history of seed size. Science 307:576–580.
Müller KF (2005) SeqState – primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 4:65–69
Müller K, Albach DC (2010) Evolutionary rates in Veronica L. (Plantaginaceae): Disentangling the influence of life history and breeding system. J Molec Evol 70:44–56
Müller KF, Borsch T, Hilu KW (2006) Phylogenetic utility of rapidly evolving DNA at high taxonomical levels: Contrasting matK, trnT-F, and rbcL in basal angiosperms. Molec Phylogen Evol 41:99–117
Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67
Paradis E (2006) Analysis of phylogenetics and evolution with R. Springer, New York
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.
Press MC, Graves JD, Stewart GR (1988) Transpiration and carbon acquisition in root hemiparasitic angiosperms. J Exp Bot 39:1009–1014
R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org
Rees M, Venable DL (2007): Why do big plants make big seeds? J Ecol 95:926–936
Ronquist F (1997) Dispersal-vicariance analysis: A new approach to the quantification of historical biogeography. Syst Biol 46:195–203.
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Schluter D, Price T, Mooers, AO, Ludwig D (1997) Likelihood of ancestral states in adaptive radiation. Evolution 51:1699–1711
Selosse M-A, Bauer R, Moyersoen B (2002) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytol 155:183–195
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu WS, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer J Bot 92:142–166
Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–81
Strykstra RJ, Bekker RM, van Andel J (2002) Dispersal and life span spectra in plant communities: a key to safe site dynamics, species coexistence and conservation. Ecography 25:145–160
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, Massachusetts
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
Tank DC, Olmstead RG (2008) From annuals to perennials: phylogeny of subtribe Castillejinae (Orobanchaceae). Amer J Bot 95:608–625
Těšitel J, Malinová T, Štech M, Herbstová M (2009) Variation in the Melampyrum sylvaticum group in the Carpathian and Hercynian region: two lineages with different evolutionary histories. Preslia 81:1–22
Turnbull LA, Rees M, Crawley MJ (1999) Seed mass and the competition/colonization trade-off: a sowing experiment. J Ecol 87:899–912
Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters DM, Webb DA (1972) Flora Europaea 3 (Diapensiaceae to Myoporaceae). Cambridge University Press, Cambridge
Van der Veken S, Bellemare J, Verheyen K, Hermy M (2007) Life-history traits are correlated with geographical distribution patterns of western European forest herb species. J Biogeogr 34:1723–1735
Vrancken J, Brochmann C, Wesselingh RA (2009) How did an annual plant react to Pleistocene glaciations? Postglacial history of Rhinanthus angustifolius in Europe. Biol J Linn Soc 98:1–13
Weber HC (1975) Vergleichende Betrachtungen über die unterirdischen Organe von Lathraea squamaria L. und Tozzia alpina L. (Scrophulariaceae). Beitr Biol Pflanzen 51:1–15
Wettstein R (1895) Der Saison-Dimorphismus als Ausgangspunkt für die Bildung neuer Arten im Pflanzenreiche. Ber Deutsch Bot Ges 13:303–313
White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA Genes for phylogenetics. In Innis N, Gelfand D, Sninsky J, White T (eds) PCR – Protocols and applications – A laboratory manual. Academic Press, New York, pp 315–322
Winkler E, Heinken T (2007) Spread of an ant-dispersed annual herb: An individual-based simulation study on population development of Melampyrum pratense L. Ecol Modelling 203:424–438
Wolfe AD, Randle CP, Liu L, Steiner KE (2005) Phylogeny and biogeography of Orobanchaceae. Folia Geobot 40:115–134
Wu MJ, Huang SF, Huang TC, Lee PF, Lin TP (2005) Evolution of the Euphrasia transmorrisonensis complex (Orobanchaceae) in alpine areas of Taiwan. J Biogeogr 32:1921–1929
Zopfi HJ (1995) Life history variation and infraspecific heterochrony in Rhinanthus glacialis (Scrophulariaceae). Pl Syst Evol 198:209–233
Zopfi HJ (1998) Life-history variation among populations of Euphrasia rostkoviana Hayne (Scrophulariaceae) in relation to grassland management. Biol J Linn Soc 64:179–205
Acknowledgements
We would like to thank Jitka Farská (Faculty of Science, University of South Bohemia) for helping with field sampling, Petr Sklenář and Jiří Hadinec (Faculty of Science, Charles University in Prague), Magnus Popp and Galina Gussarova (National Centre for Biosystematics, Oslo) for providing samples of South American Bartsia species, Tozzia alpina and East African specimens, Duncan D. Cameron (University of Sheffield) for his comments and suggestions and Jan Lepš (Faculty of Science, University of South Bohemia) for general advice on ecology of hemiparasitic plants. This study was supported by a grant IAA601410805 from the Grant Agency of the Academy of Sciences of the Czech Republic, grant 206/08/H044 from the Grant Agency of the Czech Republic and grants LC06073 and 6007665801 from the Ministry of Education of the Czech Republic.
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Těšitel, J., Říha, P., Svobodová, Š. et al. Phylogeny, Life History Evolution and Biogeography of the Rhinanthoid Orobanchaceae. Folia Geobot 45, 347–367 (2010). https://doi.org/10.1007/s12224-010-9089-y
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DOI: https://doi.org/10.1007/s12224-010-9089-y