Abstract
Gagea lutea and G. spathacea are spring geophytes naturally co-occurring in woodlands, characterised by contrasting reproductive strategies probably caused by divergent ploidy levels. The hexaploid G. lutea relies on vegetative reproduction by subterranean bulbils in young stages but completely switches to sexual reproduction once a certain bulb size is attained. The nonaploid G. spathacea seems to be sterile and reproduces only vegetatively; the plants continue to form bulbils even in the rare event of flowering. This study used AFLP genotyping to investigate the consequences of these reproductive strategies for genetic diversity. For 150 and 100 samples from three Western Pomeranian populations of G. lutea and G. spathacea, respectively, AFLP fingerprints were analysed for three different spatial scales, the patch, the transect, and the region. Applying a threshold for genotypic identity of <0.05 simple matching distance, 22–30 genets were detected in the three G. lutea populations, with all genets confined to single populations. Clonal genets consisted of 2–9 samples and extended over up to 28 m, but never occupied the whole length of a transect; 67–75% of all patches had different genets. Genetic distances between genets within populations were similar to those recorded between populations. Genotyping of G. spathacea revealed a single clonal genet for all three populations sampled within a distance of 30 km. The absent genetic diversity confirms the suspected sexual sterility. Gagea spathacea seems to be one of the few non-apomictic, fully clonal vascular plants able to occupy a significant range solely by dispersal of vegetative diaspores.
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Arnaud-Haond S, Alberto F, Teixeira S, Procaccini G, Serrao EA, Duarte CM (2005) Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Hered 96:434–440
Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139
Barrat-Segretain MH (1996) Strategies of reproduction, dispersion, and competition in river plants: a review. Vegetatio 123:13–37
Bauert MR, Kalin M, Baltisberger M, Edwards PJ (1998) No genetic variation detected within isolated relict populations of Saxifraga cernua in the Alps using RAPD markers. Mol Ecol 7:1519–1527
Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273
Brochmann C, Håpnes A (2001) Reproductive strategies in some arctic Saxifraga (Saxifragaceae), with emphasis on the narrow endemic S. svalbardensis and its parental species. Bot J Linn Soc 137:31–49
Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339–350
Douhovnikoff V, Dodd RS (2003) Intra-clonal variation and a similarity threshold for identification of clones: application to Salix exigua using AFLP molecular markers. Theor Appl Genet 106:1307–1315
Eckert CG (2002) The loss of sex in clonal plants. Evol Ecol 15:501–520
Eckert CG, Lui K, Bronson K, Corradini P, Bruneau A (2003) Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Mol Ecol 12:331–344
Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant-species. Am J Bot 74:123–131
Fay MF, Lledo MD, Kornblum MM, Crespo MB (1999) From the waters of Babylon? Populus euphratica in Spain is clonal and probably introduced. Biodiv Cons 8:769–778
Frey W, Lösch R (2004) Lehrbuch der Geobotanik. Pflanze und Vegetation in Raum und Zeit, 2nd edn. Elsevier/Spektrum Verlag, Munich
Gabrielsen TM, Brochmann C (1998) Sex after all: high levels of diversity detected in the arctic clonal plant Saxifraga cernua using RAPD markers. Mol Ecol 7:1701–1708
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
Henker H (2005) Goldsterne und Stinsenpflanzen in Mecklenburg-Vorpommern. Teil 1: Die Goldsterne von Mecklenburg-Vorpommern unter besonderer Berücksichtigung kritischer und neuer Sippen. Bot Rundbr Mecklenburg-Vorpommern 39:3–90
Hollingsworth ML, Bailey JP (2000) Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese Knotweed). Bot J Linn Soc 133:463–472
Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108:427–432
Hood GM (2009) PopTools version 3.1.1 (Excel plugin). Available online at http://www.cse.csiro.au/poptools/
Hultén E, Fries M (1986) Atlas of north European vascular plants north of the tropic of cancer. Koeltz, Switzerland
Kalheber H, Kalheber H (1966) Zum Vorkommen des Scheidigen Gelbsterns—Gagea spathacea (HAYNE) GILIB. - im Westerwald. Hess Flor Briefe 15(179):57–58
Kimpton SK, James EA, Drinnan AN (2002) Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production. Aust Syst Bot 15:485–492
Kirschner J, Stepánek J (1996) Modes of speciation and evolution of the sections in Taraxacum. Folia Geobot Phytotax 31:415–426
Ludwig G, May R, Otto C (2007) Verantwortlichkeit Deutschlands für die weltweite Erhaltung der Farn- und Blütenpflanzen—vorläufige Liste. BfN-Skripten 220:1–102
Lynch AJJ, Barnes RW, Cambecedes J, Vaillancourt RE (1998) Genetic evidence that Lomatia tasmanica (Proteaceae) is an ancient clone. Aust J Bot 46:25–33
Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Mesícek J, Hrouda L (1974) Chromosome numbers in Czechoslovak species of Gagea (Liliaceae). Folia Geobot 9:359–368
Meusel HE, Jäger EJ, Weinert E (1965) Vergleichende Chorologie der zentraleuropäischen Flora. Fischer, Jena
Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends Ecol Evol 14:389–394
Peakall R, Ebert D, Scott LJ, Meagher PF, Offord CA (2003) Comparative genetic study confirms exceptionally low genetic variation in the ancient and endangered relictual conifer, Wollemia nobilis (Araucariaceae). Mol Ecol 12:2331–2343
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
Peruzzi L (2008) Hybridity as a main evolutionary force in the genus Gagea Salisb. (Liliaceae). Plant Biosyst 142:179–184
Peruzzi L, Peterson A, Tison J-M, Peterson J (2008) Phylogenetic relationships of Gagea Salisb. (Liliaceae) in Italy, inferred from molecular and morphological data matrixes. Plant Syst Evol 276:219–234
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 Phyl Evol 46:446–465
Peterson A, Harpke D, Peruzzi L, Levichev IG, Tison J-M, Peterson J (2009) Hybridization drives speciation in Gagea (Liliaceae). Plant Syst Evol 278:133–148
Peterson A, Harpke D, Peruzzi L, Tison J-M, John H, Peterson J (2010) Gagea bohemica (Liliaceae), a highly variable monotypic species within Gagea sect. Didymobulbos. Plant Biosyst 144:308–322
Pfeiffer T (2007) Vegetative multiplication and patch colonisation of Asarum europaeum subsp. europaeum L. (Aristolochiaceae) inferred by a combined morphological and molecular study. Flora 202:89–97
Pfeiffer T, Günzel C, Frey W (2008) Clonal reproduction, vegetative multiplication and habitat colonisation in Tussilago farfara (Asteraceae): a combined morpho-ecological and molecular study. Flora 203:281–291
Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859
Rogstad SH, Keane B, Beresh J (2002) Genetic variation across VNTR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecol 161:111–121
Ronsheim ML (1997) Distance-dependent performance of asexual progeny in Allium vineale (Liliaceae). Am J Bot 84:1279–1284
Rozenfeld AF, Arnaud-Haond S, Hernandez-Garcia E, Eguiluz VM, Matias MA, Serrao E, Duarte CM (2007) Spectrum of genetic diversity and networks of clonal organisms. J Roy Soc Interface 4:1093–1102
Schnittler M, Eusemann P (2010) Consequences of genotyping errors for estimation of clonality—a case study from Populus euphratica Oliv. (Salicaceae). Evol Ecol 24:1417–1432
Schnittler M, Pfeiffer T, Harter D, Hamann A (2009) Bulbils contra seeds: reproductive investment in two species of Gagea (Liliaceae). Plant Syst Evol 279:29–40
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
Seybold S (1998) Gagea spathacea (Hayne) Salisbury 1806. In: Sebald O, Seybold S, Philippi G, Wright KM (eds) Die Farn- und Blütenpflanzen Baden-Württembergs. Verlag Eugen Ulmer, Stuttgart, pp 110–111
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792
Sneath PHA, Sokal RR (1973) Numerical taxonomy—the principles and practice of numerical classification. Freeman, San Francisco, p 573
Stein N, Herren G, Keller B (2001) A new DNA extraction method for high-throughput marker analysis in a large-genome species such as Triticum aestivum. Plant Breed 120:354–356
Swofford DL (2002) PAUP*—phylogenetic analysis using parsimony (* and other methods), version 4.0b10. Sinauer, Massachusetts
Tomovic G, Niketic M (2005) Gagea spathacea (Hayne) Salisb. (Liliaceae)—a new species for the flora of Serbia. Arch Biol Sci 57:291–294
Tsujimura N, Ishida K (2008) Isozyme variation under different modes of reproduction in two clonal winter annuals, Sedum rosulato-bulbosum and Sedum bulbiferum (Crassulaceae). Plant Species Biol 23:71–80
Urbanska KM (1992) Populationsbiologie der Pflanzen. Grundlagen, Probleme, Perspektiven. Gustav Fischer, Stuttgart
Weber E (1996) Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobot Phytotax 31:373–380
Welk E (2002) Arealkundliche Analyse und Bewertung der Schutzrelevanz seltener und gefährdeter Gefäßpflanzen Deutschlands. Schriftenreihe Vegetationskunde 37:1–337
Westergård M (1936) A cytological study of Gagea spathacea (with a note on the chromosome number and embryo-sac formation in Gagea minima). C R Trav Lab Carlsbergv 21:437–451
Ziegenhagen B, Bialozyt R, Kuhlenkamp V, Schulze I, Ulrich A, Wulf M (2003) Spatial patterns of maternal lineages and clones of Galium odoratum in a large ancient woodland: inferences about seedling recruitment. J Ecol 91:578–586
Acknowledgments
We want to thank Susanne Starke and several student collaborators for their help in sampling; David Harter, Noreen Formella, and Anna Roschanski for help with DNA extraction and AFLP reactions; and Dr Igor Levichev and Dr Angela Peterson for sharing and discussion of ideas. Permission from environmental authorities (Staatliches Amt für Umwelt und Natur Ueckermünde) to collect plant material in the nature reserve “Eldena” is gratefully acknowledged. This study was supported by a Käthe-Kluth scholarship of the Ernst-Moritz-Arndt-University Greifswald to T.P.
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Pfeiffer, T., Klahr, A., Heinrich, A. et al. Does sex make a difference? Genetic diversity and spatial genetic structure in two co-occurring species of Gagea (Liliaceae) with contrasting reproductive strategies. Plant Syst Evol 292, 189–201 (2011). https://doi.org/10.1007/s00606-010-0404-0
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DOI: https://doi.org/10.1007/s00606-010-0404-0