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Lack of genetic structure and evidence for long-distance dispersal in ash (Fraxinus excelsior) populations under threat from an emergent fungal pathogen: implications for restorative planting

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Abstract

Genetic analysis on populations of European ash (Fraxinus excelsior) throughout Ireland was carried out to determine the levels and patterns of genetic diversity in naturally seeded trees in ash woodlands and hedgerows, with the aim of informing conservation and replanting strategies in the face of potential loss of trees as a result of ash dieback. Samples from 33 sites across Northern Ireland and three sites in the Republic of Ireland were genotyped for eight nuclear and ten chloroplast microsatellites. Levels of diversity were high (mean A R = 10.53; mean H O = 0.709; mean H E = 0.765) and were similar to those in Great Britain and continental Europe, whilst levels of population genetic differentiation based on nuclear microsatellites were extremely low (Φ ST = 0.0131). Levels of inbreeding (mean F IS = 0.067) were significantly lower than those reported for populations from Great Britain. Fine-scale analysis of seed dispersal indicated potential for dispersal over hundreds of metres. Our results suggest that ash woodlands across Ireland could be treated as a single management unit, and thus native material from anywhere in Ireland could be used as a source for replanting. In addition, high potential for dispersal has implications for recolonization processes post-ash dieback (Chalara fraxinea) infection, and could aid in our assessment of the capacity of ash to shift its range in response to global climate change.

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References

  • Ashley MV (2010) Plant parentage, pollination and dispersal: how DNA microsatellites have altered the landscape. Crit Rev Plant Sci 29:148–161

    Article  CAS  Google Scholar 

  • Augspurger C (1983) Recruitment around tropical trees: changes in cohort distance with time. Oikos 40:189–196

    Article  Google Scholar 

  • Bacles CFE, Burczyk J, Lowe AJ, Ennos RA (2005) Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59:979–990

    PubMed  Google Scholar 

  • Bacles CFE, Lowe AJ, Ennos RA (2006) Effective seed dispersal across a fragmented landscape. Science 311:628

    Article  PubMed  Google Scholar 

  • Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity 101:368–380

    Article  CAS  PubMed  Google Scholar 

  • Brachet S, Jubier MF, Richard M, Jung-Muller B, Frascaria-Lacoste N (1999) Rapid identification of microsatellite loci using 5’ anchored PCR in common ash Fraxinus excelsior. Mol Ecol Notes 8:160–163

    CAS  Google Scholar 

  • Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen, pp 298–312

    Google Scholar 

  • Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed Central  PubMed  Google Scholar 

  • DeSalle R, Amato G (2004) The expansion of conservation genetics. Nat Rev Genet 5:702–712

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:1–15

    Google Scholar 

  • Ebert D, Peakall R (2009a) Chloroplast simple sequence repeats (cpSSRs): technical resources and recommendations for expanding cpSSR discovery and applications to a wide array of plant species. Mol Ecol Resour 9:673–690

    Article  CAS  PubMed  Google Scholar 

  • Ebert D, Peakall R (2009b) A new set of universal de novo sequencing primers for extensive coverage of noncoding chloroplast DNA: new opportunities for phylogenetic studies and cpSSR discovery. Mol Ecol Resour 9:777–783

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Ferrazzini D, Monteleoni I, Belletti P (2007) Genetic variability and divergence among Italian populations of common ash (Fraxinus excelsior L.). Ann For Sci 64:159–168

    Article  Google Scholar 

  • Forget PM, Wenny D (2005) How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal. In: Forget PM et al (eds) Seed fate: seed predation, seed dispersal and seedling establishment. CABI Publishing, Wallingford, pp 379–393

    Chapter  Google Scholar 

  • FRAXIGEN (2005) Ash species in Europe: biological characteristics and practical guidelines for sustainable use. Oxford Forestry Institute, Oxford

    Google Scholar 

  • Garcia C, Jordano P, Godoy JA (2007) Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction. Mol Ecol 16:1947–1955

    Article  CAS  PubMed  Google Scholar 

  • Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283

    Article  CAS  PubMed  Google Scholar 

  • Gérard PR, Temunovic M, Sannier J, Bertolino P, Dufour J, Frascaria-Lacoste N, Fernández-Manjarrés JF (2013) Chilled but not frosty: understanding the role of climate in the hybridization between the Mediterranean Fraxinus angustifolia Vahl and the temperate Fraxinus excelsior L. (Oleaceae) ash trees. J Biogeogr 40:835–846

    Article  Google Scholar 

  • Godefroid S, Piazza C, Rossi G et al (2011) How successful are plant species reintroductions? Biol Conserv 144:672–682

    Article  Google Scholar 

  • Goudet J (2001) Fstat, version 2.9.3, A program to estimate and test gene diversities and fixation indices. http://www2.unil.ch/popgen/softwares/fstat.htm

  • Grivet D, Robledo-Arnuncio JJ, Smouse PE, Sork VL (2009) Relative contribution of contemporary pollen and seed dispersal to the neighbourhood size of a seedling population of California valley oak (Quercus lobata, Née). Mol Ecol 16:3967–3979

    Article  Google Scholar 

  • Harbourne ME, Douglas GC, Waldren S, Hodkinson TR (2005) Characterization and primer development and amplification of chloroplast microsatellite regions of Fraxinus excelsior. J Plant Res 118:339–341

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Maggia L, Bandou E, Breyne P, Caron J, Chevallier MH, Doligez A, Dutech C, Kremer A, Latouche-Hallé C, Troispoux V, Veron V, Degen B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 neotropical tree species. Mol Ecol 15:559–571

    Article  CAS  PubMed  Google Scholar 

  • Hebel I, Haas R, Dounavi A (2006) Genetic variation of common ash (Fraxinus excelsior L.) populations from provenance regions in southern Germany by using nuclear and chloroplast microsatellites. Silvae Genetica 55:38–44

    Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Herbert R, Samuel S, Pattison G (1999) Using local stock for planting native trees and shrubs. Forestry Commission Practice Note 8. Forestry Commission, Edinburgh, UK

  • Heuertz M, Hausman J-F, Tsvetkov I, Frascaria-Lacoste N, Vekemans X (2001) Assessment of genetic structure within and among Bulgarian populations of common as (Fraxinus excelsior L.). Mol Ecol 10:1615–1623

    Article  CAS  PubMed  Google Scholar 

  • Heuertz M, Vekemans X, Hausman J-F, Palada M, Hardy OJ (2003) Estimating seed vs. pollen dispersal from spatial genetic structure in the common ash. Mol Ecol 12:2483–2495

    Article  CAS  PubMed  Google Scholar 

  • Heuertz M, Fineschi S, Anzidei M et al (2004a) Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol Ecol 13:3437–3452

    Article  CAS  PubMed  Google Scholar 

  • Heuertz M, Hausman J-F, Hardy OJ, Vendramin GG, Frascaria-Lacoste N, Vekemans X (2004b) Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior). Evolution 58:976–988

    PubMed  Google Scholar 

  • Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228

    Article  Google Scholar 

  • Janzen D (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Article  Google Scholar 

  • Jones N, Burley J (1973) Seed certification, provenance nomenclature and genetic history in forestry. Silvae Genetica 23:53–58

    Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program Cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kowalski T (2006) Chalara fraxinea sp nov associated with dieback of ash (Fraxinus excelsior) in Poland. For Pathol 36:264–270

    Article  Google Scholar 

  • Lefort F, Brachet S, Frascaria-Lacoste N, Edwards KJ, Douglas GC (1999) Identification and characterization of microsatellite loci in ash (Fraxinus excelsior L.) and their conservation in the olive family. Mol Ecol Notes 8:1088–1090

    Article  CAS  Google Scholar 

  • Levine JM, Murrell DJ (2003) The community-level consequences of seed dispersal patterns. Annu Rev Ecol Evol Syst 34:549–574

    Article  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understorey shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Marigo G, Peltier J-P, Girel J, Pautou G (2000) Success in the demographic expansion of Fraxinus excelsior L. Trees 15:1–13

    Article  Google Scholar 

  • Morand ME, Brachet S, Rossignol P, Dufour J, Frascaria-Lacoste N (2002) A generalised heterozygote deficiency assessed with microsatellites in French common ash populations. Mol Ecol 11:377–385

    Article  CAS  PubMed  Google Scholar 

  • Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285

    Article  PubMed  Google Scholar 

  • Pautasso M, Aas G, Queloz V, Holdenreider O (2013) European as (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Conserv 158:37–49

    Article  Google Scholar 

  • Powell W, Machray GC, Provan J (1996) Polymorphism revealed by simple sequence repeats. Trends Plant Sci 1:215–222

    Article  Google Scholar 

  • Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and systematic. Trends Ecol Evol 16:142–147

    Article  PubMed  Google Scholar 

  • Queloz V, Grüning CR, Berndt R, Kowalski T, Sieber TN, Holdenreider O (2011) Cryptic speciation in Hymenoscyphus albidus. For Pathol 41:133–142

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GenePop (version 1.2): population genetic software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed Central  PubMed  Google Scholar 

  • Smouse PE, Sork VL, Scofield DG, Grivet D (2012) Using seedling and pericarp tissues to determine maternal parentage of dispersed valley oak recruits. J Hered 103:250–259

    Article  PubMed  Google Scholar 

  • Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landsc Ecol 21:821–836

    Article  Google Scholar 

  • Steinitz O, Troupin D, Vendramin GG, Nathan R (2011) Genetic evidence for a Janzen-Connell recruitment pattern in reproductive offspring of Pinus halepensis trees. Mol Ecol 20:4152–4164

    Article  CAS  PubMed  Google Scholar 

  • Sutherland BG, Belaj A, Nier S, Cottrell JE, Vaughan SP, Hubert J, Russell K (2010) Molecular biodiversity and population structure in common ash (Fraxinus excelsior L.) in Britain: implications for conservation. Mol Ecol 19:2196–2211

    Article  CAS  PubMed  Google Scholar 

  • Thomasset M, Fernández-Manjarrés JF, Douglas GC, Bertolino P, Frascaria-Lacoste N, Hodkinson TR (2013) Assignment testing reveals multiple introduced source populations including potential ash hybrids (Fraxinus excelsior x F. angustifolia) in Ireland. Eur J For Res 132:195–209

    Article  Google Scholar 

  • Thomasset M, Hodkinson TR, Restoux G, Frascaria-Lacoste N, Douglas GC, Fernández-Manjarrés JF (2014) Thank you for not flowering: conservation genetics and gene flow analysis of native and non-native populations of Fraxinus (Oleaceae) in Ireland. Heredity 112:596–606

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analysis in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Wang BC, Smith TB (2002) Closing the seed dispersal loop. Trends Ecol Evol 17:379–385

    Article  Google Scholar 

  • Wardle P (1961) Biological flora of the British Isles: Fraxinus excelsior L. J Ecol 49:739–751

    Article  Google Scholar 

  • Webber J (1981) A natural biological control of Dutch elm disease. Nature 292:449–451

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast and nuclear DNAs. Proc Natl Acad Sci U S A 84:9054–9058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ziegenhagen B, Liepelt S, Kuhlenkamp V, Fladung M (2003) Molecular identification of individual oak and fir trees from maternal tissues of their fruits or seeds. Trees 17:345–350

    CAS  Google Scholar 

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Acknowledgments

We are grateful to four anonymous referees, whose suggestions and comments greatly improved an earlier draft of the manuscript. This study was funded by the Natural Heritage Research Partnership (NHRP) between the Northern Ireland Environment Agency (NIEA) and Quercus, Queen’s University Belfast (QUB). Thanks to Dr Philip Perrin, Botanical, Environmental & Conservation (BEC) Consultants Ltd., for providing data on the location and composition of ash woodlands in the Republic of Ireland and Kieran Coyle for assistance with leaf collection. John Farren acted as NIEA Client Officer.

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Authors and Affiliations

  1. Quercus, School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK

    Gemma E. Beatty, W. Ian Montgomery, Neil Reid, David G. Tosh & Jim Provan

  2. School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK

    Gemma E. Beatty, James A. Brown, Eamon M. Cassidy, Caroline M. V. Finlay, Lorraine McKendrick, W. Ian Montgomery, Neil Reid, David G. Tosh & Jim Provan

  3. Institute for Global Food Security, Queen’s University Belfast, Belfast, UK

    Jim Provan

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  1. Gemma E. Beatty
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  2. James A. Brown
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  3. Eamon M. Cassidy
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  4. Caroline M. V. Finlay
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Correspondence to Jim Provan.

Additional information

Communicated by Z. Kaya

This article is part of the Topical collection on Population structure

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Table S1

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Table S2

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Table S3

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Fig. S1

Network showing relationships between the eight cpSSR haplotypes observed. Each mutation is shown by a dash, with the locus and allele size change indicated. An alternative homoplasious linkage between haplotypes H2 and H7 is indicated by the dashed line. (PPTX 41 kb)

Fig. S2

Correlograms of autocorrelation coefficient (θ; y-axis) plotted against distance (x-axis). 95 % confidence intervals are indicated by dashed red lines. Note that in some correlograms, the first two distance intervals (0 – 50 m and 50 – 100 m) may be at a different scale to subsequent intervals. (PPTX 125 kb)

Fig. S3

Example of large allele dropout in consecutive individuals at locus M230. Note that in both cases, the large allele has not been called by the genotyping software. (PPTX 122 kb)

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Beatty, G.E., Brown, J.A., Cassidy, E.M. et al. Lack of genetic structure and evidence for long-distance dispersal in ash (Fraxinus excelsior) populations under threat from an emergent fungal pathogen: implications for restorative planting. Tree Genetics & Genomes 11, 53 (2015). https://doi.org/10.1007/s11295-015-0879-5

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  • DOI: https://doi.org/10.1007/s11295-015-0879-5

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