Knowing the level of genetic diversity and structure in marginal plant populations is essential for managing their genetic resources. This is particularly important for rare scattered tree species, such as Sorbus torminalis (L.) Crantz. We investigated the genetic diversity and its spatial distribution in peripheral populations of S. torminalis. As the species is known to reproduce vegetatively, we also evaluated clonal structure within populations. Using 13 nuclear microsatellite loci designed in two multiplexes, we genotyped 172 individuals revealing the existence of 100 distinct genotypes. Number of ramets per genotype was variable across populations with an average of 1.72. Examples of somaclonal variation at particular loci were detected. Measures of genetic diversity of the total sample were relatively high (mean allelic richness AR = 10.293; expected heterozygosity He = 0.756), as compared to other S. torminalis populations. We noticed a slightly negative inbreeding coefficient (FIS = -0.029) indicating a small excess of heterozygotes, which is typical for self-incompatible plants. Genetic differentiation among populations was low (FST = 0.048), but Bayesian clustering methods revealed the existence of three distinct genetic clusters only in part related to population structure. Significant spatial genetic structure within populations was also detected (Sp = 0.0125) indicating fine-scale pattern of isolation by distance. Our study demonstrated that peripheral populations of S. torminalis may exhibit relatively high levels of genetic diversity despite the existence of vegetative propagation. Nevertheless, if the studied or similar populations are expected to be utilized as seed sources for ex-situ or in-situ conservation purposes, the existence of clonal structure and spatial genetic structure must be taken into account in order to avoid excessive sampling of the same or closely related genets.
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Jankowska-Wroblewska S, Meyza K, Sztupecka E, Kubera L, Burczyk J (2016). Clonal structure and high genetic diversity at peripheral populations of Sorbus torminalis (L.) Crantz.. iForest 9: 892-900. - doi: 10.3832/ifor1885-009
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Andrea Piotti
Paper history
Received: Sep 27, 2015
Accepted: Feb 02, 2016
First online: May 29, 2016
Publication Date: Dec 14, 2016
Publication Time: 3.90 months
© SISEF - The Italian Society of Silviculture and Forest Ecology 2016
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(1)
Ally D, Ritland K, Otto S (2008)Can clone size serve as a proxy for clone age? An exploration using microsatellite divergence in
Populus tremuloides. Molecular Ecology 17: 4897-4911.
CrossRef |
Gscholar
(2)
Ally D, Ritland K, Otto SP (2010)Aging in a long-lived clonal tree. PLoS Biology 8: e1000454.
CrossRef |
Gscholar
(3)
Angelone S, Hilfiker K, Holderegger R, Bergamini A, Hoebee S (2007)Regional population dynamics define the local genetic structure in
Sorbus torminalis. Molecular Ecology 16: 1291-1301.
CrossRef |
Gscholar
(4)
Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA (2007)Standardizing methods to address clonality in population studies. Molecular Ecology 16: 5115-5139.
CrossRef |
Gscholar
(5)
Assis J, Castilho Coelho N, Alberto F, Valero M, Raimondi P, Reed D, Serrao EA (2013)High and distinct range-edge genetic diversity despite local bottlenecks. PloS ONE 8: e68646.
CrossRef |
Gscholar
(6)
Bakker EG, Van Dam BC, Van Eck HJ, Jacobsen E (2001)The description of clones of
Quercus robur L. and
Q. petraea (Matt.) Liebl. with microsatellites and AFLP in an ancient woodland. Plant Biology 3: 616-621.
CrossRef |
Gscholar
(7)
Balloux F, Lugon-Moulin N (2002)The estimation of population differentiation with microsatellite markers. Molecular Ecology 11: 155-165.
CrossRef |
Gscholar
(8)
Bednorz L (2004)Rozmieszczenie i zasoby
Sorbus torminalis (Rosaceae: Maloideae) w Polsce [Distribution and resources of
Sorbus torminalis (Rosaceae: Maloideae) in Poland]. Fragmenta Floristica et Geobotanica Polonica 11: 105-121. [in Polish]
Gscholar
(9)
Bednorz L (2007)Conservation of genetic resources of
Sorbus torminalis in Poland. Dendrobiology 58: 3-7.
Online |
Gscholar
(10)
Bednorz L, Myczko L, Kosinski P (2006)Genetic variability and structure of the wild service tree (
Sorbus torminalis (L.) crantz) in Poland. Silvae Genetica 55: 197-202.
Online |
Gscholar
(11)
Belletti P, Monteleone I, Ferrazzini D (2007)A population genetic study in a scattered forest species, wild service tree [
Sorbus torminalis (L.) Crantz], using RAPD markers. European Journal of Forest Research 127: 103-114.
CrossRef |
Gscholar
(12)
Chybicki IJ, Burczyk J (2009)Simultaneous estimation of null alleles and inbreeding coefficients. Journal of Heredity 100: 106-113.
CrossRef |
Gscholar
(13)
Corander J, Marttinen P (2006)Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology 15: 2833-2843.
CrossRef |
Gscholar
(14)
Corander J, Marttinen P, Siren J, Tang J (2008)Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9: 539.
CrossRef |
Gscholar
(15)
Demesure B, Le Guerroue B, Lucchi G, Prat D, Petit RJ (2000)Genetic variability of a scattered temperate forest tree:
Sorbus torminalis L. (Crantz). Annals of Forest Science 57: 63-71.
CrossRef |
Gscholar
(16)
Demesure-Musch B, Oddou-Muratorio S (2004)EUFORGEN technical guidelines for genetic conservation and use for wild service tree (
Sorbus torminalis). Bioversity International, Rome, Italy, pp. 6.
Online |
Gscholar
(17)
Dering M, Chybicki IJ, Raczka G (2015)Clonality as a driver of spatial genetic structure in populations of clonal tree species. Journal of Plant Research 128: 731-745.
CrossRef |
Gscholar
(18)
Doyle JJ, Doyle JH (1990)Isolation of plant DNA from fresh tissue. Focus 12: 13-15.
Gscholar
(19)
Earl DA, Von Holdt BM (2012)STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359-361.
CrossRef |
Gscholar
(20)
Eckert CG, Samis KE, Lougheed SC (2008)Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Molecular Ecology 17: 1170-1188.
CrossRef |
Gscholar
(21)
Ellstrand NC, Elam DR (1993)Population genetic consequences of small population-size - implications for plant conservation. Annual Review of Ecology and Systematics 24: 217-242.
CrossRef |
Gscholar
(22)
Estoup A, Jarne P, Cornuet JM (2002)Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology 11: 1591-1604.
CrossRef |
Gscholar
(23)
Evanno G, Regnaut S, Goudet J (2005)Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620.
CrossRef |
Gscholar
(24)
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.
Online |
Gscholar
(25)
Falush D, Stephens M, Pritchard JK (2007)Inference of population structure using multilocus genotype data: dominant markers and null alleles. Moleculat Ecology Notes 7: 574-578.
CrossRef |
Gscholar
(26)
García-Ramos G, Kirkpatrick M (1997)Genetic models of adaptation and gene flow in peripheral populations. Evolution 51: 21-28.
CrossRef |
Gscholar
(27)
George JP, Konrad H, Collin E, Thevenet J, Ballian D, Idzojtic M, Kamm U, Zhelev P, Geburek T (2015)High molecular diversity in the true service tree (
Sorbus domestica) despite rareness: data from Europe with special reference to the Austrian occurrence. Annals of Botany 115 (7): 1105-1115.
CrossRef |
Gscholar
(28)
Gianfranceschi L, Seglias N, Tarchini R, Komjanc M, Gessler C (1998)Simple sequence repeats for the genetic analysis of apple. Theoretical and Applied Genetics 96 (8): 1069-1076.
CrossRef |
Gscholar
(29)
González-González EA, González-Pérez MA, Rivero E, Sosa PA (2010)Isolation and characterization of microsatellite loci in
Sorbus aria (Rosaceae). Conservation Genetics Resources 2: 341-343.
CrossRef |
Gscholar
(30)
Goudet J (1995)FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity 86: 485-486.
Online |
Gscholar
(31)
Gross CL, Nelson PA, Haddadchi A, Fatemi M (2012)Somatic mutations contribute to genotypic diversity in sterile and fertile populations of the threatened shrub,
Grevillea rhizomatosa (Proteaceae). Annals of Botany 109: 331-342.
CrossRef |
Gscholar
(32)
Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit R (2011)Current trends in microsatellite genotyping. Molecular Ecology Resources 11 (4): 591-611.
CrossRef |
Gscholar
(33)
Hardy OJ, Vekemans X (2002)SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618-620.
CrossRef |
Gscholar
(34)
Hedhly A, Hormaza JI, Herrero M (2009)Global warming and sexual plant reproduction. Trends in Plant Science 14: 30-36.
CrossRef |
Gscholar
(35)
Hoebee SE, Menn C, Rotach P, Finkeldey R, Holderegger R (2006)Spatial genetic structure of
Sorbus torminalis: the extent of clonal reproduction in natural stands of a rare tree species with a scattered distribution. Forest Ecology and Management 226: 1-8.
CrossRef |
Gscholar
(36)
Hoebee SE, Arnold U, Duggelin C, Gugerli F, Brodbeck S, Rotach P, Holderegger R (2007)Mating patterns and contemporary gene flow by pollen in a large continuous and a small isolated population of the scattered forest tree
Sorbus torminalis. Heredity 99: 47-55.
CrossRef |
Gscholar
(37)
James EA, McDougall KL (2014)Spatial genetic structure reflects extensive clonality, low genotypic diversity and habitat fragmentation in
Grevillea renwickiana (Proteaceae), a rare, sterile shrub from south-eastern Australia. Annals of Botany 114: 413-423.
CrossRef |
Gscholar
(38)
Jolivet C, Degen B (2011)Spatial genetic structure in wild cherry (
Prunus avium L.): II. Effect of density and clonal propagation on spatial genetic structure based on simulation studies. Tree Genetics and Genomes 7: 541-552.
CrossRef |
Gscholar
(39)
Jump AS, Marchant R, Penuelas J (2009)Environmental change and the option value of genetic diversity. Trends in Plant Science 14: 51-58.
CrossRef |
Gscholar
(40)
Kalinowski ST, Wagner AP, Taper ML (2006)ML-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6: 576-579.
CrossRef |
Gscholar
(41)
Kalinowski ST, Taper ML, Marshall TC (2007)Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16: 1099-1106.
CrossRef |
Gscholar
(42)
Kamm U, Rotach P, Gugerli F, Siroky M, Edwards P, Holderegger R (2009)Frequent long-distance gene flow in a rare temperate forest tree (
Sorbus domestica) at the landscape scale. Heredity 103: 476-482.
CrossRef |
Gscholar
(43)
Klekowski EJ (2003)Plant clonality, mutation, diplontic selection and mutational meltdown. Biological Journal of the Linnean Society 79: 61-67.
CrossRef |
Gscholar
(44)
Koskela J, Buck A, Teissier du Cros E (2007)Climate change and forest genetic diversity: implications for sustainable forest management in Europe. Bioversity International, Rome, Italy, pp. 111.
Online |
Gscholar
(45)
Kramer AT, Havens K (2009)Plant conservation genetics in a changing world. Trends in Plant Science 14: 599-607.
CrossRef |
Gscholar
(46)
Kučerová V, Honec M, Paule L, Zhelev P, Gömöry D (2010)Genetic differentiation of
Sorbus torminalis in Eastern Europe as determined by microsatellite markers. Biologia 65: 817-821.
CrossRef |
Gscholar
(47)
Lesica P, Allendorf FW (1995)When are peripheral populations valuable for conservation? Conservation Biology 9: 753-760.
CrossRef |
Gscholar
(48)
Lian C, Oishi R, Miyashita N, Hogetsu T (2004)High somatic instability of a microsatellite locus in a clonal tree,
Robinia pseudoacacia. Theoretical and Applied Genetics 108: 836-841.
CrossRef |
Gscholar
(49)
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van De Weg E, Gessler C (2002)Development and characterisation of 140 new microsatellites in apple (
Malus x domestica Borkh.). Molecular Breeding 10: 217-241.
CrossRef |
Gscholar
(50)
Loiselle BA, Sork VL, Nason J, Graham C (1995)Spatial genetic structure of a tropical understory shrub,
Psychotria officinalis (Rubiaceae). American Journal of Botany 82: 1420.
CrossRef |
Gscholar
(51)
Ludwig S, Robertson A, Rich TC, Djordjevic M, Cerovic R, Houston L, Harris SA, Hiscock SJ (2013)Breeding systems, hybridization and continuing evolution in Avon Gorge
Sorbus. Annals of Botany 111 (4): 563-575.
CrossRef |
Gscholar
(52)
Mock KE, Rowe CA, Hooten MB, Dewoody J, Hipkins VD (2008)Clonal dynamics in western North American aspen (
Populus tremuloides). Molecular Ecology 17: 4827-4844.
CrossRef |
Gscholar
(53)
Nagamitsu T, Ogawa M, Ishida K, Tanouchi H (2004)Clonal diversity, genetic structure, and mode of recruitment in a
Prunus ssiori population established after volcanic eruptions. Plant Ecology 174: 1-10.
CrossRef |
Gscholar
(54)
Oddou-Muratorio S, Guesnet D, Ozdemir E, Petit RJ, Demesure B (2001a)Patterns of seed dispersal in a scattered forest tree species (
Sorbus torminalis) based on multi-scale investigation of population genetic structure for chloroplast DNA. In: “Genetic Response of Forest Systems to Changing Environmental Conditions” (Müller-Starck G, Schubert R eds). Forestry Sciences vol. 70, Springer, Netherlands, pp. 271-280.
CrossRef |
Gscholar
(55)
Oddou-Muratorio S, Aligon C, Decroocq S, Plomion C, Lamant T, Mush-Demesure B (2001b)Microsatellite primers for
Sorbus torminalis and related species. Molecular Ecology Notes 1 (4): 297-299.
CrossRef |
Gscholar
(56)
Oddou-Muratorio S, Houot ML, Demesure-Musch B, Austerlitz F (2003)Pollen flow in the wild service tree,
Sorbus torminalis (L.) Crantz. I. Evaluating the paternity analysis procedure in continuous populations. Molecular Ecology 12: 3427-3439.
CrossRef |
Gscholar
(57)
Oddou-Muratorio S, Demesure-Musch B, Pelissier R, Gouyon PH (2004)Impacts of gene flow and logging history on the local genetic structure of a scattered tree species,
Sorbus torminalis L. Crantz. Molecular Ecology 13: 3689-3702.
CrossRef |
Gscholar
(58)
Oddou-Muratorio S, Klein EK (2008)Comparing direct
vs. indirect estimates of gene flow within a population of a scattered tree species. Molecular Ecology 17: 2743-2754.
CrossRef |
Gscholar
(59)
Ortego J, Bonal R, Munoz A (2010)Genetic consequences of habitat fragmentation in long-lived tree species: the case of the mediterranean Holm Oak (
Quercus ilex L.). Journal of Heredity 101: 717-726.
CrossRef |
Gscholar
(60)
Ozolinčius R, Lekevičius E, Stakenas V, Galvonaite A, Samas A, Valiukas D (2013)Lithuanian forests and climate change: possible effects on tree species composition. European Journal of Forest Research 133 (1): 51-60.
CrossRef |
Gscholar
(61)
O’Connell L, Ritland K (2004)Somatic mutations at microsatellite loci in western redcedar (
Thuja plicata: Cupressaceae). Journal of Heredity 95: 172-176.
CrossRef |
Gscholar
(62)
Pritchard JK, Stephens M, Donnelly P (2000)Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
Online |
Gscholar
(63)
Pyttel P, Kunz J, Bauhus J (2013)Growth, regeneration and shade tolerance of the Wild Service Tree (
Sorbus torminalis (L.) Crantz) in aged oak coppice forests. Trees 27: 1609-1619.
CrossRef |
Gscholar
(64)
Rasmussen KK, Kollmann J (2004)Poor sexual reproduction on the distribution limit of the rare tree
Sorbus torminalis. Acta Oecologica 25: 211-218.
CrossRef |
Gscholar
(65)
Rasmussen KK, Kollmann J (2007a)Genetic diversity, spatial patterns, and growth of root sprouts in a temperate tree at the northern distribution limit. Ecoscience 14: 250-258.
CrossRef |
Gscholar
(66)
Rasmussen KK, Kollmann J (2007b)Low genetic diversity in small peripheral populations of a rare European tree (
Sorbus torminalis) dominated by clonal reproduction. Conservation Genetics 9: 1533-1539.
CrossRef |
Gscholar
(67)
Rich T, Houston L, Robertson A, Proctor M (2010)Whitebeams, rowans and service trees of Britain and Ireland. A monograph of British and Irish Sorbus L. BSBI Handbook no. 14, Botanical Society of the British Isles, London, UK, pp. 229.
Gscholar
(68)
Schnittler M, Eusemann P (2010)Consequences of genotyping errors for estimation of clonality: a case study on
Populus euphratica Oliv. (Salicaceae). Evolutionary Ecology 24: 1417-1432.
CrossRef |
Gscholar
(69)
Stoeckel S, Masson JP (2014)The exact distributions of F(IS) under partial asexuality in small finite populations with mutation. PloS ONE 9: e85228.
CrossRef |
Gscholar
(70)
Stoeckel S, Grange J, Fernandez-Manjarres JF, Bilger I, Frascaria-Lacoste N, Mariette S (2006)Heterozygote excess in a self-incompatible and partially clonal forest tree species -
Prunus avium L. Molecular Ecology 15: 2109-2118.
CrossRef |
Gscholar
(71)
Tarnawski A (2001)Jarzab brekinia w regionie grudziadzkim [Wild service tree in the region Grudziadz]. SAR POMORZE - Bydgoszcz, Grudziadz, Poland, pp. 48.
Gscholar
(72)
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006)The genome of black cottonwood,
Populus trichocarpa (Torr. & Gray). Science 313 (5793): 1596-1604.
CrossRef |
Gscholar
(73)
Vallejo-Marín M, Dorken ME, Barrett SCH (2010)The ecological and evolutionary consequences of clonality for plant mating. Annual Review of Ecology, Evolution, and Systematics 41: 193-213.
CrossRef |
Gscholar
(74)
Vaughan SP, Cottrell JE, Moodley DJ, Connolly T, Russell K (2007)Clonal structure and recruitment in British wild cherry (
Prunus avium L.). Forest Ecology and Management 242: 419-430.
CrossRef |
Gscholar
(75)
Vekemans X, Hardy OJ (2004)New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13: 921-935.
CrossRef |
Gscholar
(76)
Wagner V, Durka W, Hensen I (2011)Increased genetic differentiation but no reduced genetic diversity in peripheral
vs. central populations of a steppe grass. American Journal of Botany 98: 1173-1179.
CrossRef |
Gscholar
(77)
Wang J (2011)Unbiased relatedness estimation in structured populations. Genetics 187: 887-901.
CrossRef |
Gscholar
(78)
Wilk JA, Kramer AT, Ashley MV (2009)High variation in clonal
vs. sexual reproduction in populations of the wild strawberry,
Fragaria virginiana (Rosaceae). Annals of Botany 104: 1413-1419.
CrossRef |
Gscholar
(79)
Wyman J, Bruneau A, Tremblay M-F (2003)Microsatellite analysis of genetic diversity in four populations of
Populus tremuloides in Quebec. Canadian Journal of Botany 81: 360-367.
CrossRef |
Gscholar
(80)
Yakimowski SB, Eckert CG (2008)Populations do not become less genetically diverse or more differentiated towards the northern limit of the geographical range in clonal
Vaccinium stamineum (Ericaceae). New Phytologist 180: 534-544.
CrossRef |
Gscholar
(81)
Young A, Boyle T, Brown T (1996)The population genetic consequences of habitat fragmentation for plants. Trends in Ecology and Evolution 11: 413-418.
CrossRef |
Gscholar
