Genetic Diversity of Orchid Malaxis monophyllos Over European Range as an Effect of Population Properties and Postglacial Colonization

• Autorzy: Jermakowicz E. , Brzosko E. , Kotowicz J. , Wróblewska A.

Identyfikatory

DOI

10.3161/15052249PJE2017.65.1.007

• Języki publikacji: EN

Abstrakty

EN

Malaxis monophyllos is a rare orchid with a fragmented boreal-montane distribution in Europe where it is associated with both natural swampy and anthropogenic habitats. We employed extensive sampling of M. monophyllos populations from different habitat types, over its whole European geographic range, to examine its genetic diversity patterns and phylogeographic structure using amplified fragment length polymorphisms (AFLPs). Our results revealed the relatively low genetic diversity of M. monophyllos, with the effect of small population sizes and inbreeding as the driving forces operating within the European part of its range. The statistically highest values of genetic diversity were found in populations from the boreal region (average: percentage of polymorphic loci PPL₃ = 21.6%, Nei's gene diversity H_j3 = 0.144, the rarity index DW₃ = 1.34), while populations from mountainous regions were characterised by a reduced level of genetic diversity (e.g. an average for Alpine populations: PPL₃ = 18.1%, H_j3 = 0.121, DW₃ = 0.84) in comparison to boreal ones. Our results revealed that the newly established anthropogenic populations in the Polish uplands were probably founded from numerous external sources and should be considered a significant source of the species' genetic diversity. We also confirmed the low genetic differentiation among M. monophyllos populations (F_ST = 0.074), with the lack of distinguishable genetic clusters, that supports results about the multidirectional gene flow between M. monophyllos populations in Europe, and directed conservation efforts on conserving all suitable for this species habitats.

Słowa kluczowe

EN

AFLPs; amplified fragment length polymorphisms; anthropogenic habitats; boreal-montane species; glacial refugia; Orchidaceae

PL

AFLPs; amplifikacja polimorfizmu długości fragmentu; siedliska antropogeniczne; gatunki borealne; gatunki północno-górskie; refleksje lodowcowe; Orchidaceae; storczykowate

• Wydawca: Museum and Institute of Zoology, Polish Academy of Sciences
• Czasopismo: Polish Journal of Ecology
• Rocznik: 2017
• Tom: Vol. 65, nr 1
• Strony: 69--86
• Opis fizyczny: Bibliogr. 92 poz., mapa, rys., tab., wykr.

Twórcy

autor

Jermakowicz E.

• Institute of Biology, University of Bialystok, K. Ciołkowskiego 1J, 15-245 Bialystok, Poland

autor

Brzosko E.

• Institute of Biology, University of Bialystok, K. Ciołkowskiego 1J, 15-245 Bialystok, Poland

autor

Kotowicz J.

• Faculty of Mathematics and Informatics, University of Bialystok, Ciołkowskiego 1M, 15-245 Bialystok, Poland

autor

Wróblewska A.

• Institute of Biology, University of Bialystok, K. Ciołkowskiego 1J, 15-245 Bialystok, Poland

Bibliografia

• [1] Ackerman J. D. 2007 — Invasive orchids: weeds we hate to love? — Lankesteriana, 7: 19–21.
• [2] Alsos I. G., Ehrich D., Thuiller W., Eidesen P. B., Tribsch A., Schönswetter P., Lagaye C., Taberlet P., Brochmann C. 2012 — Genetic consequences of climate change for northern plants — P. Roy. Soc. Lond. B. 279: 2042–2051.
• [3] Bernacki L., Babczyńska-Sendek B., Tokarska-Guzik B., Sobierajska J. 1991 — Nowe stanowiska Malaxis monophyllos (L.) Swarz (Orchidaceae) na Wyżynie Śląskiej i terenach sąsiednich [New stands of Malaxis monophyllos (L.) Swarz (Orchidaceae) at the Silesian Upland and neighboring areas] — Acta Biologia Silesiana. Florystyka i geografia roślin, 19: 43–53 (in Polish).
• [4] Berthouly-Salazar C., Hui C., Blackburn T. M., Gaboriaud C., Van Rensburg B., Van Vuuren B. J., Le Roux J. J. 2013 — Long-distance dispersal maximizes evolutionary potential during rapid geographical range expansion — Mol. Ecol. 22: 5793–5804.
• [5] Bhagwat S. A., Willis K. J. 2008 — Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? — J. Biogeogr. 35: 464–482.
• [6] Bonin A., Bellemain E., Bronken Eidesen P., Pompanon F., Brochmann C., Taberlet P. 2004 — How to track and assess genotyping errors in population genetic studies — Mol. Ecol. 13: 3261–3273.
• [7] Brzosko E., Ratkiewicz M., Wróblewska A. 2002 — Allozyme differentiation and genetic structure of the Lady's slipper (Cypripedium calceolus) island populations in north-east Poland — Bot. J. Linn. Soc. 138: 433–440.
• [8] Brzosko E., Wróblewska A., Jermakowicz E ., Hermaniuk A. 2013 — High level of genetic variation within clonal orchid Goodyera repens — Plant Sys. Evol. 299: 1537–1548.
• [9] Brzosko E., Wróblewska A., Tałałaj I., Adamowski W. 2009 — Patterns of genetic diversity in Platanthera bifolia (Orchidaceae) with respect to life history traits and recent range expansion — Folia Geobot. 44: 131–144.
• [10] Cai X., Feng Z., Zhang X., Xu W., Hou B., Ding X. 2011 — Genetic diversity and population structure of an endangered Orchid (Dendrobium loddigesii Rolf) from China revealed by SRAP markers — Sci. Horti., Amsterdam, 129: 877–881.
• [11] Cameron K. M. 2005 — Leave it to the leaves: a molecular phylogenetic study of Malaxideae (Epidendroideae, Orchidaceae) — Am. J. Bot. 92: 1025–1032.
• [12] Charlesworth D., Charlesworth B. 1995 — Quantitative Genetics in Plants: The Effect of the Breeding System on Genetic Variability — Evolution, 49: 911–920.
• [13] Chung M. Y., Nason J. D., López-Pujol J., Yamashiro T., Yang B-Y., Luo Y.-B., Chung M. G. 2014 — Genetic consequences of fragmentation on populations of the terrestrial orchid Cymbidium goeringii — Biol. Conserv. 170: 222–231.
• [14] Claessens J., Kleynen J. 2011 — The flower of the European Orchid. Form and function — Published by Jean Claessens and Jacques Kleynen, 137–145.
• [15] Comes H. P., Kadereit J. W. 1998 — The effect of Quaternary climatic changes on plant distribution and evolution — Trends Plant Sci. 3: 432–438.
• [16] Crawford R. M. M. 2008 — Cold climate plants in warmer world — Plant Ecology & Diversity, 1: 285–297.
• [17] Davis M. B., Shaw R. G. 2001 — Range shifts and adaptive responses to Quaternary Climate Changes — Science, 292: 673–679.
• [18] Diez H. F., Grosjean M., Graumlich L. 2003 — Climate variability and change in high elevation regions: past, present and future — Climatic Change, 59: 1–4.
• [19] Duminil J., Fineschi S., Hampe A., Jordano P., Salvini D., Vendramin G. G., Petit R. J. 2007 — Can population genetic structure be predicted from life-history traits? — Am. Nat. 169: 662–672.
• [20] Ehrich D. 2006 — AFLPdat: a collection of R functions for convenient handling of AFLP data — Mol. Ecol. Notes, 6: 603–604.
• [21] Ehrich D., Alsos J. G., Brochmann C. 2008 — Where did the northern peatland species survive the dry glacials: cloudberry (Rubus chamaemorus) as an example — J. Biogeogr. 35: 801–814.
• [22] Eidesen P. B., Ehrich D., Bakkestuen V., Alsos I. G., Gilg O., Taberlet P., Brochmann C. 2013 — Genetic roadmap of the Arctic: plant dispersal highways, traffic barriers and capitals of diversity — New Phytol. 200: 898–910.
• [23] Ellstrand N. C. 2014 — Is gene flow the most important evolutionary force in plants? — Am. J. Bot. 101: 737–753.
• [24] Embleton C. 1984 — Geomorphology of Europe. — Macmillan, London, 429 pp.
• [25] Esfeld K., Hensen I., Wesche K., Jakob S., Tischew S., Blatter F. R. 2008 — Molecular data indicate independent colonizations of former lignite mining areas in Eastern Germany by Epipactis palustris (Orchidaceae) — Biodivers. Conserv. 17: 2441–2453.
• [26] Evanno G., Regnaut S., Goudet J. 2005 — Detecting the number of clasters of individuals using the software Structure: a simulation study — Mol. Ecol. 14: 2611–2620.
• [27] Excoffier L., Laval G., Schneider S. 2005 — Arlequin (version 3.0): an integrated software package for population genetics data analyses Evolutionary Bioinformatics Online, 1: 47–50.
• [28] Falush D., Stephens M., Prichard J. K. 2003 — Inference of population structure using multilocus genotype data: linked loci and correlated alleles frequencies — Genetics, 164: 1567–1587.
• [29] Felsenstein J. 1993 — PHYLIP (PHYLogeny Inference Package) version 3.6, — Distributed by the author, Department of Genetics, University of Washington, Seattle, WA.
• [30] Forrest A. D., Hollingsworth M. L., Hollingsworth P. M., Sydes C., Bateman R. M. 2004 — Population genetic structure in European populations of Spiranthes romanzoffiana set in the context of other genetic studies on orchids — Heredity, 92: 218–227.
• [31] Frankham R. 1996 — Relationship of genetic variation to population size in wildlife — Conserv. Biol. 10: 1500–1508.
• [32] Franks S. J., Weber J. J., Aitken S. N. 2013 — Evolutionary and plastic responses to climate change in terrestrial plant populations — Evol. Appl. 7: 123–139.
• [33] Gentili R., Bacchetta G., Fenu G., Cogoni D., Abeli T., Rossi G., Salvatore M.C., Baroni C., Citterio S. 2015 — From cold to warm-stage refugia for boreal-alpine plants in southern European and Mediterranean mountains: the last chance to survive or an opportunity for speciation? — Biodiversity, DOI:10.1080/1488 8386.2015.1116407.
• [34] Hampe A., Petit R. J. 2005 — Conserving biodiversity under climate change: the rear edge matters — Ecology Letters, 8: 461–467.
• [35] Hamrick J. L., Godt M. J. W. 1996 — Effects of life history traits on genetic diversity in plant species — Philos. T. R. Soc. Lond. B. 351: 1291–1298.
• [36] Hedberg K. O. 1992 — Taxonomic differentiation in Saxifraga hirculus L. (Saxifragaceae) — a circumpolar Arctic-Boreal species of Central Asiatic origin — Bot. J. Linn. Soc. 109: 377–393.
• [37] Helsen K., Jacquemyn H., Hermy M., Vandepitte K., Honnay O. 2013 — Rapid buildup of genetic diversity in founder populations of the gynodioecious plant species Origanum vulgare after semi-natural grassland restoration. — PLoS ONE 8: e67255. DOI: 10.1371/journal.pone.0067255.
• [38] Hewitt G. M. 2004 — Genetic consequences of climatic oscillation in the Quaternary — Philos. T. R. Soc. Lond. B. 359: 183–195.
• [39] Hollingsworth P. M, Dickson J. H. 1997 — Genetic variation in rural and urban populations of Epipactis helleborine (L.) Crantz. (Orchidaceae) in Britain — Bot. J. Linn. Soc. 123: 321–331.
• [40] Holsinger K. E., Lewis P. O. 2003 — Hickory v. 1.0. Storrs, CT: Department of Ecology & Evolutionary Biology, University of Connecticut. Available at: http://www.eeb.uconn.edu/.
• [41] Holub J., Procházka F. 2000 — Red List of vascular plants of the Czech Republic — Preslia Praha, 72, 203 pp.
• [42] Hornemann G., Michalski S. G., Durka W. 2012 — Short-term fitness and long-term population trends in the orchid Anacamptis morio — Plant Ecol. 213: 1157–1164.
• [43] Hultén E., Fries M. 1986 — Atlas of North European Vascular Plants. II. — Koeltz Scientific Books Königstein.
• [44] Huson H., Bryant D. 2006 — Application of phylogenetic networks in evolutionary studies — Mol. Biol. Evol. 23: 254–267.
• [45] Ilves A., Metsare M., Tali K., Kull T. 2015 — The impact of recent colonization on the genetic diversity and fine-scale genetic structure in Orchis militaris — Plant Sys. Evol. 301: 1875–1886.
• [46] Jacquemyn H., Vandepitte K., Brys R., Honnay O., Roldán-Ruiz I. 2007 — Fitness variation and genetic diversity in small, remnant populations of the food deceptive orchid Orchis purpurea — Biol. Conserv. 139: 203–210.
• [47] Jacquemyn H., Brys R., Adriaens D., Honnay O., Roldán-Ruiz I. 2009 — Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula — Conserv. Genet. 10: 161–168.
• [48] Jermakowicz E., Brzosko E. 2016 — Demographic responses of boreal-montane orchid Malaxis monophyllos (L.) Sw. populations to contrasting environmental conditions. — Acta Soc. Bot. Pol. 85: 3488. http://dx.doi.org/10.5586/asbp.3488.
• [49] Jermakowicz E., Ostrowiecka B., Tałałaj I., Kostro-Ambroziak A., Pliszko A. 2015a — Male and female reproductive success in natural and anthropogenic populations of Malaxis monophyllos (L.) Sw. (Orchidaceae) — Biodiversity: Research and Conservation, 39: 37–44.
• [50] Jermakowicz E., Wróblewska A., Brzosko E., Mirski P., Hirse T. 2015b — Phylogeographic structure of the boreal-mountain orchid Malaxis monophyllos (L.) Sw. as a result of multi-directional gene flow — Bot. J. Linn. Soc. 178: 138–154.
• [51] Jersáková J., Malinová T. 2007 — Spatial aspects of seed dispersal and seedling recruitment in orchids — New Phytol. 176: 448–459.
• [52] Jump A. S., Peñuelas J. 2005 — Running to stand still: adaptation and the response of plants to rapid climate change — Ecology Letters, 8: 1010–1020.
• [53] Kalas J. A., Viken A., Bakken T. 2006 — Norwegian Red List — Art Data Banken.
• [54] Kaźmierczakowa R., Zarzycki K., Mirek Z. 2014 — Polish Red Data Book of Plants. Pteridophytes and flowering plants — Instytut Ochrony Przyrody PAN, Kraków 895 pp.
• [55] Kramp K., Huck S., Niketić M. G., Tomović G., Schmitt T. 2009 — Multiple glacial refugia and complex postglacial range shifts of the obligatory woodland plant Polygonatum verticillatum (Convallariaceae — Plant Biology, 11: 392–404.
• [56] Krüger A. M., Hellwig F. H., Oberprieler C. 2002 — Genetic diversity in natural and anthropogenic inland populations of salt-tolerant plants: random amplified polymorphic DNA analyses of Aster tripolium L. (Compositae) and Salicornia ramosissima Woods (Chenopodiaceae) — Mol. Ecol. 11: 1647–1655.
• [57] Latałowa M. 2003 — Holocen [Holocene] (In: Palinologia [Palynology], Eds: S. Dybova-Jachowicz, A. Sadowska) — Wydawnictwa Instytutu Botaniki PAN, Kraków, (in Polish).
• [58] Leimu R., Mutikainen P., Koricheva J., Fischer M. 2006 — How general are positive relationships between plant population size, fitness and genetic variation? — J. Ecol. 94: 942–952.
• [59] Lienert J. 2004 — Habitat fragmentation effects on fitness of plant populations — a review — J. Nat. Conserv. 12: 53–72.
• [60] Michl T., Huck S., Schmitt T., Liebrich A., Haase P., Büdel B. 2010 — The molecular population structure of the tall forb Cicerbita alpine (Asteraceae) supports the idea of cryptic glacial refugia in central Europe — Bot. J. Linn. Soc. 164: 142–154.
• [61] Murren C. J. 2003 — Spatial and demographic population genetic structure in Catasetum viridiflavum across a human-disturbed habitat — J. Evol. Biol. 16: 333–342.
• [62] Nogués-Bravo D., Araujo M. B., Errea M. P., Martinez-Rica J. P. 2007 — Exposure of global mountain systems to climate warming during the 21st Century — Glob. Environ. Change, 17: 420–428.
• [63] Nordström S., Hedrén M. 2008 — Genetic differentiation and postglacial migration of the Dactylorhiza majalis ssp. traunsteineri/lapponica complex into Fenoscandia — Plant Sys. Evol. 276: 73–87.
• [64] Nowak A. 2006 — Sozophytes (red-listed species) in Silesian anthropogenic habitats and their role in nature conservation — Biodiversity: Research and Conservation, 3–4: 386–390.
• [65] Obidowicz A., Ralska-Jasiewiczowa M., Kupryjanowicz M., Latałowa M., Nalepka D. 2004 — Picea abies (L.) H. Karst — Spruce (In: Late Glacial and Holocene history of vegetation in Poland based on isopollen maps, Eds: M. Ralska-Jasiewiczowa, M. Latałowa, K. Wasilikowa, K. Tobolski, E. Madeyska, H. E. Wright, Ch. Turner) — Kraków: W. Szafer Institute of Botany, Polish Academy of Science, 147–158.
• [66] Parmesan C. 2006 — Ecological and evolutionary responses to recent climate change — Ann Review in Ecology, Evolution and Systematics, 37: 637–669.
• [67] Pánek T., Hradecký J. 2016 (Eds.) — Landscapes and Landforms of the Czech Republic — Springer International Publishing, Switzerland.
• [68] Paulus S. U., Nowak C., Bálint M., Pfenninger M.. 2013 — The impact of global climate change on genetic diversity within populations and species — Mol. Ecol. 22: 925–946.
• [69] Peakall R., Smouse P. E. 2012 — GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research — an update — Bioinformatics, 28: 2537–2539.
• [70] Pellissier L., Eidsen P. B., Ehrich D., Descombes P., Schönswetter P., Tribsch A., Westergaard K. B., Alvarez N., Guisan G., Zimmermann N. E., Normand S., Vittoz P., Luoto M., Domgaard Ch., Brochmann Ch., Wisz M. S., Alsos I. G. 2015 — Past climate-driven range shifts and population genetic diversity in arctic plants — J. Biogeogr. 43: 461–470.
• [71] Petit R. J., Duminil J., Fineschi S., Hampe A., Salvini D., Vendramin G. G. 2005 — Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations — Mol. Ecol. 14: 689–701.
• [72] Phillips R. D., Dixon K. W., Peakall R. 2012 — Low population genetic differentiation in the Orchidaceae: implications for the diversification of the family — Mol. Ecol. 21: 5208–5220.
• [73] Pillon Y., Qamaruz-Zaman F., Fay M. F., Hendoux F., Piquot Y. 2007 — Genetic diversity and ecological differentiation in the endangered fen orchid (Liparis loeselii) — Conserv. Genet. 8: 177–184.
• [74] Pritchard J. K., Wen X., Falush D. 2009 — STRUCTURE v. 2.3 — University of Chicago, Chicago, USA. http://pritch.bsd.uchicago.edu.
• [75] Recart W., Ackerman J. D., Cuevas A. A. 2013 — There goes the neighborhood: apparent competition between invasive and native orchids mediated by a specialist florivorous weevil — Biol. Invasions, 15: 283–293.
• [76] Ronikier M. 2011 — Biogeography of high-mountains plants in the Carpathians: an emerging phylogeographical perspective — Taxon, 60: 372–389.
• [77] Saitou N, Nei M. 1987 — The neighbor-joining method: a new method for reconstructing phylogenetic trees — Mol. Biol. Evol. 4: 406–425.
• [78] Scacchi R., De Angelis G., Corbo R. M. 1991 — Effect of the breeding system on the genetic structure in three Cephalanthera spp. (Orchidaceae) — Plant Sys. Evol. 176: 53–61.
• [79] Schefferson R. P., Kull T., Tali K. 2008 — Mycorrhizal interactions of orchids colonizing Estonian mine tailing hills — Am. J. Bot. 95: 156–164.
• [80] Schönswetter P., Popp M., Brochmann Ch. 2006 — Central Asian origin of and strong genetic differentiation among populations of the rare and disjunct Carex atrofusca (Cyperaceae) in the Alps — J. Biogeogr. 33: 948–956.
• [81] Schönswetter P., Tribsch A. 2005 — Vicariance and dispersal in the alpine perennial Bupleurum stellatum L. (Apiaceae) — Taxon, 54: 725–732.
• [82] STATISTICA StatSoft Inc. 2011 — STATISTICA User's Guide, Version 10 Fulsa — StatSoft Inc., Kraków.
• [83] Swarts N. D., Dixon K. W. 2009 — Terrestrial orchid conservation in the age of extinction — Ann. Bot. 104: 543–556.
• [84] 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.
• [85] Thuiller W., Lavorel S., Araujo M. B., Sykes M. T., Prentice I. C. 2005 — Climate change threat to plant diversity in Europe — P. Natl A. Sci. 102: 8245–8250.
• [86] Tremblay R. L., Ackerman J. D., Zimmerman J. K., Calvo R. N. 2005 — Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification — Biol. J. Linn. Soc. 84: 1–54.
• [87] Vakhrameeva M. G., Tatarenko I. V., Varlygina T. I., Torosyan G. K., Zagulski M. N. 2008 — Orchids of Russia and adjacent countries (within the borders of the former USSR). — A. R. G. Ganter Verlag, Ruggell/Lichtensten, 417–420, 612.
• [88] Vanden Broeck A., Van Landuyt W., Cox K., De Bruyn L., Gyselings R., Oostermeijer G., Valentin B., Bozic G., Dolinar B., Illyés Z., Margeay J. 2014 — High levels of effective long-distance dispersal may blur ecotypic divergence in a rare terrestrial orchid — BMC Ecol. 14: 20. www.biomedcentral.com/1472-6785/14/20.
• [89] Vos P., Hoger R., Bleeker M., Reijans M., van de Lee T., Horne M., Frijters A., Pot J., Peleman J., Kuiper M., Zabeau M. 1995 — AFLP: a new technique for DNA fingerprinting — Nucleic Acids Res. 23: 4407–4414.
• [90] Williams J. L., Jacquemyn H., Ochocki B. M., Brys R., Miller T. E. X. 2015 — Life history evolution under climate change and its influence on the population dynamic of a long-lived plant — J. Ecol. 103: 798–808.
• [91] Wróblewska A. 2012 — The role of disjunction and postglacial population expansion on phylogeographical history and genetic diversity of the circumboreal plant Chamaedaphne calyculata — Biol. J. Linn. Soc. 105: 761–775.
• [92] Young A., Boyle T., Brown T. 1996 — The population genetic consequences of habitat fragmentation for plants — Trends Ecol. Evol. 11: 413–419.

Uwagi

Opracowanie ze środków MNiSW w ramach umowy 812/P-DUN/2016 na działalność upowszechniającą naukę (zadania 2017).