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European Journal of Forest Research

, Volume 131, Issue 4, pp 1055–1069 | Cite as

Mating patterns and pollen dispersal in four contrasting wild cherry populations (Prunus avium L.)

  • Céline Jolivet
  • Aki M. Höltken
  • Heike Liesebach
  • Wilfried Steiner
  • Bernd Degen
Original Paper

Abstract

Although pollen dispersal has been extensively studied in trees, parameters influencing between-population variation are still poorly understood. In this study, we conducted paternity analyses on open-pollinated seeds in four natural populations of wild cherry (Prunus avium) with contrasting density and clonal propagation, using eight microsatellite loci and one self-incompatibility system locus. We also measured four quantitative traits and spatial positions as potential correlates of reproductive success. Levels of polyandry differed among populations and 30% of the seed families exhibited unequal paternal contributions, suggesting variation in reproductive success rather than variation in mate availability. Mating occurred preferentially among neighbours in all populations, suggesting that it is a common pattern in wild cherry and probably results from pollinator behaviour. Paternal success was positively correlated with diameter at breast height, as indicated in previous studies and tree dominance only resulted in higher paternal success in low density plots. Mating patterns were thus also affected by both density and tree size. Large-scale studies are needed to disentangle relative influences of these factors on the mating system and pollination success.

Keywords

Prunus avium Self-incompatibility system Reproductive success Pollen dispersal Asexual reproduction Density 

Notes

Acknowledgments

We thank Alexandra Meier, Volker Schneck and Thomas Stauber for technical assistance, Dina Führmann for editing, Alexandre Sebbenn, Sheila Ward, Jutta Buschbom and two anonymous reviewers for constructive comments on the manuscript. This work was supported by the German Ministry of Food, Agriculture and Consumer Protection (BMELV) [grant 05/BE003/2 “Erfassung der genetischen Struktur der Vogelkirsche Prunus avium als Grundlage für ein genetisches Monitoring wichtiger Waldbaumarten in Deutschland”].

Supplementary material

10342_2011_576_MOESM1_ESM.pdf (92 kb)
Supplementary material 1 (PDF 93 kb)

References

  1. Armbruster WS, Rogers DG (2004) Does pollen competition reduce the cost of inbreeding? Am J Bot 91:1939–1943PubMedCrossRefGoogle Scholar
  2. Bacles CFE, Jump AS (2011) Taking a tree’s perspective on forest fragmentation genetics. Trends Plant Sci 16:13–18PubMedCrossRefGoogle Scholar
  3. Burczyk J (1996) Variance effective population size based on multilocus gamete frequencies in coniferous populations: an example of a Scots pine clonal seed orchard. Heredity 77:74–82CrossRefGoogle Scholar
  4. Burczyk J, Adams WT, Shimizu JY (1996) Mating patterns and pollen dispersal in a natural knobcone pine (Pinus attenuata Lemmon) stand. Heredity 77:251–260Google Scholar
  5. Burke JM, Bulger MR, Wesselingh RA, Arnold ML (2000) Frequency and spatial patterning of clonal reproduction in Louisiana iris hybrid populations. Evolution 54:137–144PubMedGoogle Scholar
  6. Byrne M, Elliott CP, Yates C, Coates DJ (2007) Extensive pollen dispersal in a bird-pollinated shrub, Calothamnus quadrifidus, in a fragmented landscape. Mol Ecol 16:1303–1314PubMedCrossRefGoogle Scholar
  7. Calzoni GL, Speranza A (1998) Insect controlled pollination in Japanese plum (Prunus salicina Lindl.). Sci Hortic 72:227–237CrossRefGoogle Scholar
  8. Chapman RE, Wang J, Bourke AFG (2003) Genetic analysis of spatial foraging patterns and resource sharing in bumble bee pollinators. Mol Ecol 12:2801–2808PubMedCrossRefGoogle Scholar
  9. Cottrell JE, Vaughan SP, Connolly T, Sing L, Moodley DJ, Russell K (2009) Contemporary pollen flow, characterization of the maternal ecological neighbourhood and mating patterns in wild cherry (Prunus avium L.). Heredity 103:118–128PubMedCrossRefGoogle Scholar
  10. De Cuyper B, Sonneveld T, Tobutt KR (2005) Determining self-incompatibility genotypes in Belgian wild cherries. Mol Ecol 14:945–955PubMedCrossRefGoogle Scholar
  11. Degen B, Bandou E, Caron H (2004) Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana. Heredity 93:585–591PubMedCrossRefGoogle Scholar
  12. Dick CW, Etchelecu G, Austerlitz F (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12:753–764PubMedCrossRefGoogle Scholar
  13. Dirlewanger E, Cosson P, Tavaud M et al (2002) Development of microsatellite markers in peach (Prunus persica L. Batsch) and their use in genetic diversity analysis in peach and sweet cherry (Prunus avium L.). Theor Appl Genet 105:127–138PubMedCrossRefGoogle Scholar
  14. Dow BD, Ashley MV (1998) Factors influencing male mating success in bur oak, Quercus macrocarpa. New For 15:161–180CrossRefGoogle Scholar
  15. Ducci F, Santi F (1997) The distribution of clones in managed and unmanaged populations of wild cherry (Prunus avium). Can J For Res 27:1998–2004CrossRefGoogle Scholar
  16. Dumolin S, Demesure B, Petit RJ (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256CrossRefGoogle Scholar
  17. Gomory D (2004) Mutual links of demographic and genetic processes in a wild cherry population during the colonization. Biologia 59:493–500Google Scholar
  18. Gonzalez-Martinez SC, Gerber S, Cervera MT et al (2002) Seed gene flow and fine-scale structure in a Mediterranean pine (Pinus pinaster Ait.) using nuclear microsatellite markers. Theor Appl Genet 104:1290–1297PubMedCrossRefGoogle Scholar
  19. Granger AR (2004) Gene flow in cherry orchards. Theorl Appl Genet 108:497–500CrossRefGoogle Scholar
  20. Hanson TR, Brunsfeld SJ, Finegan B, Waits LP (2008) Pollen dispersal and genetic structure of the tropical tree Dipteryx panamensis in a fragmented Costa Rican landscape. Mol Ecol 17:2060–2073PubMedCrossRefGoogle Scholar
  21. Höltken AM (2005). Genetische Untersuchungen zu den Vorassetzungen und Konsequenzen einer rezedenten Lebensweise am Beispiel der Vogelkirsche (Prunus avium L.). PhD Thesis, University of GöttingenGoogle Scholar
  22. Höltken AM, Gregorius HR (2006) Detecting local establishment strategies of wild cherry (Prunus avium L.). BMC Ecol 4:13CrossRefGoogle Scholar
  23. Hormaza JI, Herrero M (1996) Dynamics of pollen tube growth under different competition regimes. Sex Plant Repro 9:153–160CrossRefGoogle Scholar
  24. Janzen DH (1977) Note on optimal mate selection by plants. Am Nat 111:365–371CrossRefGoogle Scholar
  25. Jolivet C, Bernasconi G (2007) Within/between population crosses reveal genetic basis for siring success in Silene latifolia (Caryophyllaceae). J Evol Biol 20:1361–1374PubMedCrossRefGoogle Scholar
  26. 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 Genet Genomes 7:541–552CrossRefGoogle Scholar
  27. Jolivet C, Höltken AM, Liesebach H, Steiner W, Degen B (2011) Spatial genetic structure in wild cherry (Prunus avium L.): I. variation among natural populations of different density. Tree Genet Genomes 7:271–283CrossRefGoogle Scholar
  28. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106PubMedCrossRefGoogle Scholar
  29. Karron JD, Marshall DL (1993) Effects of environmental variation on fitness of singly and multiply sired progenies of Raphanus sativus (Brassicaceae). Am J Bot 80:1407–1412CrossRefGoogle Scholar
  30. Kaufman SR, Smouse PE, Alvarez-Buylla ER (1998) Pollen-mediated gene flow and differential male reproductive success in a tropical pioneer tree, Cecropia obtusifolia (Bertol. Moraceae): a paternity analysis. Heredity 81:164–173CrossRefGoogle Scholar
  31. Kraft G (1884) Beiträge zur Lehre von den Durchforstungen, Schlagstellungen und Lichtungshieben. Klindworth, HannoverGoogle Scholar
  32. Lacerda AEB, Kanashiro M, Sebbenn AM (2008) Long-pollen movement and deviation of random mating in a low-density continuous population of a tropical tree Hymenaea courbaril in the Brazilian Amazon. Biotropica 40:462–470CrossRefGoogle Scholar
  33. Marchese A, Tobutt KR, Raimondo A et al (2007) Morphological characteristics, microsatellite fingerprinting and determination of incompatibility genotypes of Sicilian sweet cherry cultivars. J Hortic Sci Biotechnol 82:41–48Google Scholar
  34. Marshall DL, Folsom MW (1991) Mate choice in plants—an anatomical to population perspective. Annu Rev Ecol Syst 22:37–63CrossRefGoogle Scholar
  35. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  36. Moriguchi Y, Tsuchiya S, Iwata H et al (2007) Factors influencing male reproductive success in a Cryptomeria japonica seed orchard revealed by microsatellite marker analysis. Silvae Genet 56:207–214Google Scholar
  37. Nielsen R, Tarpy DR, Reeve HK (2003) Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol Ecol 12:3157–3164PubMedCrossRefGoogle Scholar
  38. Oddou-Muratorio S, Houot ML, Demesure-Musch B, Austerlitz F (2003) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. I. Evaluating the paternity analysis procedure in continuous populations. Mol Ecol 12:3427–3439PubMedCrossRefGoogle Scholar
  39. Oddou-Muratorio S, Klein EK, Austerlitz F (2005) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Mol Ecol 14:4441–4452PubMedCrossRefGoogle Scholar
  40. Oddou-Muratorio S, Klein EK, Demesure-Musch B, Austerlitz F (2006) Real-time patterns of pollen flow in the wild-service tree, Sorbus torminalis (Rosaceae). III. Mating patterns and the ecological maternal neighbourhood. Am J Bot 93:1650–1659PubMedCrossRefGoogle Scholar
  41. Paschke M, Bernasconi G, Schmid B (2005) Effects of inbreeding and pollen donor provenance and diversity on offspring performance under environmental stress in the rare plant Cochlearia bavarica. Basic Appl Ecol 6:325–338CrossRefGoogle Scholar
  42. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Ann Rev Ecol Evol Syst 37:187–214CrossRefGoogle Scholar
  43. Pyke GH (1984) Optimal foraging theory—a critical-review. Annl Rev Ecol Syst 15:523–575CrossRefGoogle Scholar
  44. R Development Core Team (2004) R: a language and environment for statistical computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org
  45. Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228PubMedCrossRefGoogle Scholar
  46. Robledo-Amuncio JJ, Smouse PE, Gil L, Alia R (2004) Pollen movement under alternative silvicultural practices in native populations of Scots pine (Pinus sylvestris L.) in central Spain. For Ecol Manag 197:245–255CrossRefGoogle Scholar
  47. Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2007) POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Mol Ecol Notes 7:763–766CrossRefGoogle Scholar
  48. Russell K (2003) EUFORGEN Technical guidelines for genetic conservation and use for wild cherry (Prunus avium). International Plant Genetics Ressources Institute, RomeGoogle Scholar
  49. Schueler S (2005) Pollen-mediated gene flow of trees in the temperate zone. PhD Thesis, University of Hamburg, GermanyGoogle Scholar
  50. Schueler S, Tusch A, Schuster M, Ziegenhagen B (2003) Characterization of microsatellites in wild and sweet cherry (Prunus avium L.)—markers for individual identification and reproductive processes. Genome 46:95–102PubMedCrossRefGoogle Scholar
  51. Schueler S, Tusch A, Scholz F (2006) Comparative analysis of the within-population genetic structure in wild cherry (Prunus avium L.) at the self-incompatibility locus and nuclear microsatellites. Mol Ecol 15:3231–3243PubMedCrossRefGoogle Scholar
  52. Shykoff JA, Bucheli E (1995) Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum-Violaceum, a venereal-disease of plants. J Ecol 83:189–198CrossRefGoogle Scholar
  53. Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manag 197:21–38CrossRefGoogle Scholar
  54. Snow AA, Spira TP, Liu H (2000) Effects of sequential pollination on the success of “fast” and “slow” pollen donors in Hibiscus moscheutos (Malvaceae). Am J Bot 87:1656–1659PubMedCrossRefGoogle Scholar
  55. Sonneveld T, Tobutt KR, Robbins TP (2003) Allele-specific PCR detection of sweet cherry self-incompatibility (S) alleles S1 to S16 unsing consensus and allele-specific primers. Theor Appl Gent 107:1059–1070CrossRefGoogle Scholar
  56. Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc R Soc Lond B 270:569–575CrossRefGoogle Scholar
  57. Stoeckel S (2006) Impact de la propagation aséxuée et du système d’auto-incompatibilité gamétophytique sur la structuration et l’évolution de la diversité génétique d’une essence forestière entomophile et disséminée, Prunus avium L. PhD Thesis, Cemagref, FranceGoogle Scholar
  58. Stoeckel S, Grange J, Fernandez-Manjarres JF et al (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species—Prunus avium L. Mol Ecol 15:2109–2118PubMedCrossRefGoogle Scholar
  59. Testolin R, Marrazzo T, Cipriani G et al (2000) Microsatellite DNA in peach (Prunus persica L. Batsch) and its use in fingerprinting and testing the genetic origin of cultivars. Genome 43:512–520PubMedGoogle Scholar
  60. van Kleunen M, Burczyk J (2008) Selection on floral traits through male fertility in a natural plant population. Evol Ecol 22:39–54CrossRefGoogle Scholar
  61. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  62. Vaughan SP, Cottrell JE, Moodley DJ, Connolly T, Russell K (2007a) Clonal structure and recruitment in British wild cherry (Prunus avium L.). For Ecol Manag 242:419–430CrossRefGoogle Scholar
  63. Vaughan SP, Cottrell JE, Moodley DJ, Connolly T, Russell K (2007b) Distribution and fine-scale spatial-genetic structure in British wild cherry (Prunus avium L.). Heredity 98:274–283PubMedCrossRefGoogle Scholar
  64. Vaughan SP, Boskovic RI, Gisbert-Climent A, Russell K, Tobutt KR (2008) Characterisation of novel S-alleles from cherry (Prunus avium L.). Tree Genet Genomes 4:531–541CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Céline Jolivet
    • 1
  • Aki M. Höltken
    • 2
    • 4
  • Heike Liesebach
    • 1
  • Wilfried Steiner
    • 3
  • Bernd Degen
    • 1
  1. 1.Institute of Forest GeneticsJohann Heinrich von Thünen Institut (vTI)GrosshansdorfGermany
  2. 2.Department of Wood Science, World ForestryUniversity of HamburgHamburgGermany
  3. 3.Nordwestdeutsche Forstliche Versuchsanstalt Abteilung WaldgenressourcenHann. MündenGermany
  4. 4.Forstliche Versuchs-und Forschungsantalt Baden-WürttembergFreiburgGermany

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