Abstract
In plants, clonal propagation is a common reproductive strategy in parallel to sexual reproduction. It has both advantages and drawbacks, and the potential complete loss of sexual reproduction causes serious conservation concerns, especially because population maintenance then only relies on adult survival and low genetic diversity leads to decreased adaptive potential. We investigated the rare, southernmost populations of the mostly circumboreal twinflower Linnaea borealis, located in the Western Alps. Based on 105 AFLP markers and 118 leaf samples, including replicates, we estimated the genetic similarity threshold above which samples belong to a single clone. Although the species is known for extensive clonal propagation, we observed high genotypic diversity within the seven studied populations and almost all samples were genetically distinct. Nevertheless, some clonal samples were detected in two populations, separated by up to 180 m. We found a strong genetic differentiation among populations (overall Fst = 0.38), which was congruent with the previously documented high plastid diversity in the region. We therefore hypothesize that Alpine populations are relicts of the Quaternary glacial periods, when the species probably survived at these lower latitudes before colonizing Northern Europe. Regarding conservation, our results suggest that most extant plants result from sexual reproduction and that populations are not highly threatened. Nevertheless, since clones can be very long-lived and almost no seedlings were observed in recent years, events of sexual reproduction may be ancient. The current reproductive dynamics should therefore be studied to estimate e.g. pollinators activity, proportions of flowering plants, and seed set.
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References
Antos JA, Zobel DB (1984) Ecological implications of belowground morphology of nine coniferous forest herbs. Bot Gaz 145:508–517
Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139
Barrett SCH (2015) Influences of clonality on plant sexual reproduction. P Natl Acad Sci USA 112:8859–8866
Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273
Dong B-C, Alpert P, Guo W, Yu F-H (2012) Effects of fragmentation on the survival and growth of the invasive, clonal plant Alternanthera philoxeroides. Biol Invasions 14:1101–1110
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 103:1307–1315
Eckert CG (2002) The loss of sex in clonal plants. Evol Ecol 15:501–520
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 2:217–242
Eriksson O (1988) Variation in growth rate in shoot populations of the clonal dwarf shrub Linnaea borealis. Holarct Ecol 11:259–266
Eriksson O (1993) Dynamics of genets in clonal plants. Trends Ecol Evol 8:313–316
Escaravage N, Questiau S, Pornon A, Doche B, Taberlet P (1998) Clonal diversity in a Rhododendron ferrugineum L. (Ericaceae) population inferred from AFLP markers. Mol Ecol 7:975–982
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140
Gaudeul M, Taberlet P, Till-Bottraud I (2000) Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers. Mol Ecol 9:1625–1637
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
Helenurm K, Barrett SCH (1987) The reproductive biology of boreal forest herbs. II. Phenology of flowering and fruiting. Can J Bot 65:2047–2056
Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route of route to extinction? Oikos 108:427–432
Honnay O, Jacquemyn H (2008) A meta-analysis of the relation between mating system, growth form and genotypic diversity in clonal plant species. Evol Ecol 22:299–312
Honnay O, Jacquemyn H, Roldan-Ruiz I, Hermy M (2006) Consequences of prolonged clonal growth on local and regional genetic structure and fruiting success of the forest perennial Maianthemum bifolium. Oikos 112: 21–30
Klimes L, Klimesova J, Hendriks H, van Groenendael JM (1997) Clonal plant architecture: a comparative analysis of form and function. In: de Kroon H, van Groenendael JM (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 1–29
Kohn D, Ennos R (2000) Action plan research on twinflower. SNH Contract R/AC3/BAT/98/59, Final report. Scottish Natural Heritage, Perth
Kosman E, Leonard J (2005) Similarity coefficients for molecular markers in studies of genetic relationships between individuals for haploid, diploid and polyploidy species. Mol Ecol 14:415–424
Lasso A (2008) The importance of setting the right genetic distance threshold for identification of clones using amplified fragment length polymorphism: a case study with five species in the tropical plant genus Piper. Mol Ecol Resour 8:74–82
Legg C, Cowie N, Sydes C (2003) Promoting survival prospects of rare plants. Bot J Scotl 55:77–87
Lesica P, Allendorf FW (1995) When peripheral populations are valuable for conservation. Conserv Biol 9:753–760
Lin C-H, Miriti MN, Goodell K (2016) Demographic consequences of greater clonal than sexual reproduction in Dicentra canadensis. Ecol Evol 6:3871–3883
Lundemo S, Stenoien H, Savolainen O (2010) Investigating the effects of topography and clonality on genetic structuring within a large Norwegian population of Arabidopsis lyrata. Ann Bot Lond 106:243–254
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
Niva M (2003) Life history strategies in Linnaea borealis. comprehensive summaries of Uppsala dissertations from the Faculty of Science and Technology, vol 893, pp 1–21
Oborny B, Kun A (2002) Fragmentation of clones: how does it influence dispersal and competitive ability? Evol Ecol 15:319–346
Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol Ecol 14:689–701
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Provan J, Maggs CA (2012) Unique genetic variation at a species’ rear edge is under threat from global climate change. Proc R Soc B Biol Sci 279:39–47
Reusch TBH, Ehlers A, Hämmerli A, Worm B (2005) Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc Natl Acad Sci USA 102:2826–2831
Richards CL, Hamrick JL, Donovan LA, Mauricio R (2004) Unexpectedly high clonal diversity of two salt marsh perennials across a severe environmental gradient. Ecol Lett 7:1155–1162
Rohlf F (1990) NTSYS-PC: numerical taxonomy and multivariate analysis system, version 2.02. Exeter Software, New York
Rosenberg N (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Rossetto M, Gross CL, Jones R, Hunter J (2004) The impact of clonality on an endangered tree (Elaeocarpus williamsianus) in a fragmented rainforest. Biol Conserv 117:33–39
Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555
Scobie AR, Wilcock CC (2009) Limited mate availability decreases reproductive success of fragmented populations of Linnaea borealis, a rare, clonal self-incompatible plant. Ann Bot Lond 103:835–846
Silvertown J (2008) The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. Int J Plant Sci 169:157–168
Stehlik I, Holderegger R (2000) Spatial genetic structure and clonal diversity of Anemone nemorosa in late successional deciduous woodlands of Central Europe. J Ecol 88:424–435
Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
UICN France, FCBN, MNHN (2012) La Liste rouge des espèces menacées en France—Chapitre Flore vasculaire de France métropolitaine: premiers résultats pour 1000 espèces, sous-espèces et variétés. https://inpn.mnhn.fr/espece/listerouge/FR/Flore_vasculaire_metropole_1. Accessed 17 Jul 2018
Vallejo-Marin M, Dorken ME, Barrett SCH (2010) The ecological and evolutionary consequences of clonality for plant mating. Annu Rev Ecol Syst 2010:193–213
van Groenendael JM, Klimes L, Klimesova J, Hendriks RJJ (1997) Comparative ecology of clonal plants. Philos Trop R Soc B 351:1331–1339
Vandepitte K, Roldan-Ruiz I, Jacquemyn H, Honnay O (2010) Extremely low genotypic diversity and sexual reproduction in isolated populations of the self-incompatible lily-of-the-valley (Convallaria majalis) and the role of the local forest environment. Ann Bot Lond 105:769–776
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Fritjers A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Wang Z, Xie L, Prather CM, Guo H, Han G, Ma C (2018) What drives the shift between sexual and clonal reproduction of Caragana stenophylla along a climatic aridity gradient? BMC Plant Biol 18:91
Wiberg RAW, Scobie AR, A’Hara SW, Ennos RA, Cottrell JE (2016) The genetic consequences of long term habitat fragmentation on a self-incompatible clonal plant, Linnaea borealis L. Biol Conserv 201:405–413
Wilcock CC (2002) Maintenance and recovery of rare clonal plants: the case of the twinflower (Linnaea borealis L.). Bot J Scotl 54:121–131
Wilcock CC, Jennings SB (1999) Partner limitation and restoration of sexual reproduction in the clonal dwarf shrub Linnaea borealis L. (Caprifoliaceae). Protoplasma 208:76–86
Wroblewska A (2013) The phylogeographical and population genetic approach to the investigation of the genetic diversity patterns in self-incompatible clonal and polyploidy Linnaea borealis subsp. borealis. Bot J Linn Soc 173:64–76
Young AG, Broadhurst LM, Thrall PH (2012) Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability. Ann Bot Lond 109:643–653
Acknowledgements
We are grateful to the Parc National de la Vanoise, who made this project possible through a scientific partnership with, and financial support to the Muséum National d’Histoire Naturelle (MNHN). Lab work was conducted at the BoEM lab of the MNHN, except the genotyping step that was performed at the Gentyane Platform of INRA Clermont-Ferrand, France, under the responsibility of C. Poncet. We also thank G. Rouhan for his help, and two anonymous reviewers for their helpful comments on a previous version of the manuscript.
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Gaudeul, M., Delahaye, T. & Muller, S. AFLP markers show low levels of clonal propagation and high genotypic diversity in the rare, southernmost populations of Linnaea borealis L. (Caprifoliaceae) in the Western Alps. Genetica 147, 79–90 (2019). https://doi.org/10.1007/s10709-019-00054-6
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DOI: https://doi.org/10.1007/s10709-019-00054-6