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Short-distance pollen dispersal for an outcrossed, wind-pollinated southern beech (Nothofagus nervosa (Phil.) Dim. et Mil.)

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Abstract

The mating system (outcrossing, selfing, and biparental inbreeding) and the extent of pollen flow are two of the most important genetic features that determine the genetic structure of plant populations, and both are crucial for the design of conservation strategies. The objectives here were to estimate mating system parameters and to fit the pollen dispersal kernel for the southern beech, Nothofagus nervosa. We sampled 25 mothers and 372 progeny from two stands in the Tromen Lake region of Argentina. We registered spatial positions of the maternal trees, and genotyped mothers and offspring for five simple sequence repeat markers.

We estimated single-locus (t s = 0.95) and multilocus (t m = 0.99) outcrossing rates and biparental inbreeding (t m-t s = 0.04). The species is strongly outcrossing, but correlated paternity within maternal sibships (r p = 0.10) indicates that each maternal parent is sampling a different and restricted array of pollen donors. We used two protocols (twogener and kindist) to fit an exponential power dispersal kernel to the structure of pollen clouds sampled by different mothers. The estimated effective number of pollen donors contributing to a single mother was N ep = 9.9. The twogener and kindist analyses yielded slightly different estimates, but both indicated short average distances for pollen dispersal (<35 m), indicating that the dispersal kernel was strongly leptokurtic (β = 0.36). While short-distance pollen dispersal predominates, there remains a nontrivial probability of long-distance dispersal. The results are discussed in the context of ongoing conservation and management programs.

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References

  • Abramowitz M, Stegun IA (1964) Handbook of mathematical functions with formulas, graphs, and mathematical tables. U.S. Government Printing Office, Washington, DC

    Google Scholar 

  • 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 

  • Austerlitz F, Smouse PE (2001) Two-generation analysis of pollen flow across a landscape; II. Relation between Φ(ft), pollen dispersal and interfemale distance. Genetics 157:851–857

    PubMed  CAS  Google Scholar 

  • Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape: IV. Estimating the dispersal parameter. Genetics 161:355–363

    PubMed  Google Scholar 

  • Austerlitz F, Dick CW, Dutech C, Klein EK, Oddou-Muratorio S, Smouse PE, Sork VL (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13:937–954

    Google Scholar 

  • Austerlitz F, Dutech C, Smouse PE, Davis F, Sork VL (2007) Estimating anisotropic pollen dispersal: a case study in Quercus lobata. Heredity 99:193–204

    Google Scholar 

  • Azpilicueta MM, Caron H, Bodenes C, Gallo L (2004) SSR markers for analysing South American Nothofagus species. Silvae Genet 53:240–243

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bittencourt JV, Sebbenn AM (2008) Pollen movement within a continuous forest of wind-pollinated Araucaria angustifolia, inferred from paternity and twogener analysis. Conserv Genet 9:855–868

    Article  Google Scholar 

  • Burczyk J, Adams WT, Shimizu JY (1996) Mating patterns and pollen dispersal in a natural knobcone pine (Pinus attenuata Lemmon.) stand. Heredity 77:251–260

    Google Scholar 

  • Burczyk J, Lewandowski A, Chalupka W (2004) Local pollen dispersal and distant gene flow in Norway spruce (Picea abies [L.] Karst.). For Ecol Manag 197:39–48

    Article  Google Scholar 

  • Chauchard L, Bava JO, Castañeda S, Laclau P, Loguercio GA, Pantaenius P, Rusch V (2012) Manual para las buenas prácticas forestales en bosques nativos de Nordpatagonia. Ministerio de Agricultura, ganadería y Pesca, Presidencia de la Nación. Argentina, p 122

  • Clark JS (1998) Why trees migrate so fast: confronting theory with dispersal biology and the paleorecord. Am Nat 152:204–224

    Article  PubMed  CAS  Google Scholar 

  • De-Lucas AI, Robledo-Arnuncio JJ, Hidalgo E, Gonzalez-Martinez SC (2008) Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 100:390–399

    Article  PubMed  CAS  Google Scholar 

  • Degen B, Bandou E, Caron H (2004) Limited pollen dispersal and biparental inbreeding in Symphonia globulifera in French Guiana. Heredity 93:585–591

    Article  PubMed  CAS  Google Scholar 

  • Dettmann ME, Pocknall DT, Romero EJ, Zamaloa MC (1990) Nothofagidites Erdtman ex Potoni‚ 1960; a catalogue of species with notes on the paleogeographic distribution of Nothofagus Bl. (Southern Beech). New Zealand Geological Survey, Lower Hutt

    Google Scholar 

  • Di-Giovanni F, Kevan PG (1991) Factors affecting pollen dynamics and its importance to pollen contamination: a review. Can J For Res 21:1155–1170

    Article  Google Scholar 

  • 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 12:753–764

    Article  PubMed  Google Scholar 

  • Donoso C (1993) Bosques templados de Chile y Argentina. Variaci¢n, Estructura y Dinámica. Ecología Forestal. Editorial Universitaria, Chile

    Google Scholar 

  • Donoso C, Lara A (1995) Utilización de los bosques nativos en Chile: pasado, presente y futuro. In: Armesto JJ, Villagran C, Arroyo KM (eds) Ecología de los Bosques nativos de Chile. Editorial Universitaria, Santiago, pp 363–388

    Google Scholar 

  • 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 91:1253–1256

    Article  CAS  Google Scholar 

  • Dutech C, Sork VL, Irwin AJ, Smouse PE, Davis F (2005) Gene flow and fine-scale genetic structure in a wind-pollinated tree species, Quercus lobata (Fagaceaee). Am J Bot 92:252–261

    Article  PubMed  CAS  Google Scholar 

  • Dyer RJ, Sork VL (2001) Pollen pool heterogeneity in shortleaf pine. Pinus echinata Mill Mol Ecol 10:859–866

    CAS  Google Scholar 

  • Fernandez-Manjarres JF, Idol J, Sork VL (2006) Mating patterns of black oak Quercus velutina (Fagaceae) in a Missouri oak-hickory forest. J Hered 97:451–455

    Article  PubMed  Google Scholar 

  • Gallo LA, Pastorino MJ (2010) Evidence of genetic drift in neutral and adaptive genome. In: Evoltree conference “Forest ecosystem genomics and adaptation,” San Lorenzo del Escorial, Madrid, España. INIA

  • Gallo L, Donoso C, Marchelli P, Donoso P (2004) Variación en Nothofagus nervosa (Phil.) Dim. et Mil (N. alpina, N. procera). In: Donoso C, Premoli AC, Gallo L, Ipinza R (eds) Variación intraespecífica en especies arboreas de los bosques templados de Chile y Argentina. Editorial Universitaria, Santiago, pp 115–144

    Google Scholar 

  • Gallo LA, Marchelli P, Chauchard L, Penalba MG (2009) Knowing and doing: research leading to action in the conservation of forest genetic diversity of Patagonian temperate forests. Conserv Biol 23:895–898

    Article  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 

  • Hill RS, Read J (1991) A revised infrageneric classification of Nothofagus (Fagaceae). Bot J Linn Soc 105:37–72

    Article  Google Scholar 

  • Holsinger KE (2000) Reproductive systems and evolution in vascular plants. Proc Natl Acad Sci USA 97:7037–7042

    Article  PubMed  CAS  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523

    Article  PubMed  CAS  Google Scholar 

  • Klein EK, Lavigne C, Gouyon PH (2006) Mixing of propagules from discrete sources at long distance: comparing a dispersal tail to an exponential. BMC Ecol 6:3. doi:10.1186/1472-6785-6-3

    Article  PubMed  Google Scholar 

  • Koenig WD, Ashley MV (2003) Is pollen limited? The answer is blowin’ in the wind. TREE 18:157–159

    Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • Lindgren D, Paule L, Shen XH, Yazdani R, Segerström U, Wallin JE, Lejdebro ML (1995) Can viable pollen carry Scots pine genes over long distances? Grana 34:64–69

    Article  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignments methods: matching biological questions with appropriate techniques. Tree 20:136–142

    PubMed  Google Scholar 

  • Marchelli P, Gallo LA (1999) Annual and geographic variation in seed traits of Argentinean populations of southern beech Nothofagus nervosa (Phil.) Dim. et Mil. For Ecol Manag 121:239–250

    Article  Google Scholar 

  • Marchelli P, Gallo LA (2001) Genetic diversity and differentiation in a southern beech subjected to introgressive hybridization. Heredity 87:284–293

    Article  PubMed  CAS  Google Scholar 

  • Marchelli P, Gallo LA (2004) The role of glaciation, fragmentation and hybridization in shaping the distribution of the genetic variation in a Patagonian southern beech. J Biogeogr 31:451–460

    Article  Google Scholar 

  • Marchelli P, Gallo L (2006) Multiple ice-age refugia in a southern beech from southern South America as revealed by chloroplast DNA markers. Conserv Genet 7:591–603

    Article  Google Scholar 

  • Marchelli P, Caron H, Azpilicueta MM, Gallo L (2008) Primer note: a new set of highly polymorphic nuclear microsatellite markers for Nothofagus nervosa and related South American species. Silvae Genet 57:82–85

    Google Scholar 

  • Markgraf V, D’Antoni HI (1978) Pollen flora of Argentina. Modern spore and pollen types of Pteridphyta, Gymnospermae and Angiospermae. University of Arizona Press, Tucson

    Google Scholar 

  • Murawski DA, Hamrick JL (1991) The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67:167–174

    Article  Google Scholar 

  • Nason JD, Herre EA, Hamrick JL (1998) The breeding structure of a tropical keystone plant resource. Nature 391:385–687

    Article  Google Scholar 

  • Neale DB, Adams J (1985) The mating system in natural and shelterwood stands of Douglas-fir. Theor Appl Genet 71:201–207

    Google Scholar 

  • Neel JV, Ward RH (1972) The genetic structure of a tribal population, the Yanomama indians:VI. Analysis by F-statistics (including comparison with the Makiritare and Xavante). Genetics 72:639–666

    PubMed  CAS  Google Scholar 

  • Nielsen LR, Kjaer ED (2010) Gene flow and mating patterns in individuals of wych elm (Ulmus glabra) in forest and open land after the influence of Dutch elm disease. Conserv Genet 11:257–268

    Article  Google Scholar 

  • O’Connell LM, Mosseler A, Rajora OM (2006) Impacts of forest fragmentation on the mating system and genetic diversity of white spruce (Picea glauca) at the landscape level. Heredity 97:418–426

    Article  PubMed  Google Scholar 

  • Oddou-Muratorio S, Petit RJ, Le Guerroue B, Guesnet D, Demesure B (2001) Pollen- versus seed-mediated gene flow in a scattered forest tree species. Evolution 55:1123–1135

    PubMed  CAS  Google Scholar 

  • 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(14):4441–4452

    Article  PubMed  CAS  Google Scholar 

  • 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 neighborhood. Am J Bot 93:1650–1659

    Article  PubMed  Google Scholar 

  • Oddou-Muratorio S, Bontemps A, Klein EK, Chybicki IJ, Vendramin GG, Suyama Y (2010) Comparison of direct and indirect genetic methods for estimating seed and pollen dispersal in Fagus sylvatica and Fagus crenata. For Ecol Manag 259:2151–2159

    Article  Google Scholar 

  • Oddou-Muratorio S, Klein EK, Vendramin GG, Fady B (2011) Spatial vs. temporal effects on demographic and genetic structures: the roles of dispersal, masting and differential mortality on patterns of recruitment in Fagus sylvatica. Mol Ecol 20:1997–2010

    Article  PubMed  Google Scholar 

  • Okubo A, Levin SA (1989) A theoretical framework for data analysis of wind dispersal of seeds and pollen. Ecology 70:329–338

    Article  Google Scholar 

  • Pakkad G, Ueno S, Yoshimaru H (2008) Gene flow pattern and mating system in a small population of Quercus semiserrata Roxb. (Fagaceae). For Ecol Manag 255:3819–3826

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit JR, Hampe A (2006) Some evolutionary consequences of being a tree. Ann Rev Ecol Evol Syst 37:187–214

    Article  Google Scholar 

  • Pluess AR, Sork VL, Dolan B, Davis FW, Grivet D, Merg K, Papp J, Smouse PE (2009) Short distance pollen movement in a wind-pollinated tree, Quercus lobata (Fagaceae). For Ecol Manag 258:735–744

    Article  Google Scholar 

  • Puntieri J, Grosfeld JE, Heuret P (2009) Preformation and distribution of staminate and pistillate flowers in growth un its of Nothofagus alpina and N. obliqua (Nothofagaceae). Ann Bot 103:411–421

    Article  PubMed  Google Scholar 

  • Rieseberg LH, Burke JM (2001) The biological reality of species: gene flow, selection, and collective evolution. Taxon 50:47–67

    Article  Google Scholar 

  • Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228

    Article  PubMed  Google Scholar 

  • Riveros M, Parades MA, Rosas MT, Cardenas E, Armesto JJ, Arroyo KM, Palma B (1995) Reproductive biology in species of the genus Nothofagus. Environ Exp Bot 35:519–524

    Article  Google Scholar 

  • Robledo-Arnuncio JJ, Gil L (2005) Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis. Heredity 94(1):13–22

    Article  PubMed  CAS  Google Scholar 

  • Robledo-Arnuncio JJ, Garcia C (2007) Estimation of the seed dispersal kernel from exact identification of source plants. Mol Ecol 16:5098–5109

    Article  PubMed  Google Scholar 

  • Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2006) A new method of estimating the pollen dispersal curve independently of effective density. Genetics 173:1033–1045

    Article  PubMed  CAS  Google Scholar 

  • Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2007) POLDISP: a software package for indirect estimation of contemporary pollen dispersal. Mol Ecol Notes 7:763–766

    Article  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Schoen DJ, Brown AHD (1991) Intraspecific variation in population gene diversity and effective population size correlates with the mating system in plants. Proc Natl Acad Sci USA 88:4494–4497

    Article  PubMed  CAS  Google Scholar 

  • Schoen DJ, Clegg MT (1986) Monte Carlo studies of plant mating system estimation models: the one-pollen parent and mixed mating models. Genetics 112:927–945

    PubMed  CAS  Google Scholar 

  • Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manag 197:21–38

    Article  Google Scholar 

  • Smouse PE, Neel JV, Liu W (1983) Multiple-locus departures from panmictic equilibrium within and between village gene pools of Amerindian tribes at different stages of agglomeration. Genetics 104:133–153

    PubMed  CAS  Google Scholar 

  • Smouse PE, Dyer RJ, Westfall RD, Sork VL (2001) Two-generation analysis of pollen flow across a landscape: I. Male gamete heterogeneity among females. Evolution 55:260–271

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sork VL, Davis FW, Smouse PE, Apsit VJ, Dyer RJ, Fernandez JF, Kuhn B (2002) Pollen movement in declining populations of California Valley oak, Quercus lobata: where have all the fathers gone? Mol Ecol 11:1657–1668

    Article  PubMed  CAS  Google Scholar 

  • Sork VL, Smouse PE, Apsit VJ, Dyer RJ, Wetfall RD (2005) A two-generation analysis of pollen pool genetic structure in flowering dogwood, Cornus florida (Cornaceae), in the Missouri Ozarks. Am J Bot 92:262–271

    Article  PubMed  CAS  Google Scholar 

  • Streiff R, Labbe T, Bacilieri R, Steinkellner J, Grössl J, Kremer A (1998) Within population genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites. Mol Ecol 7:317–328

    Article  Google Scholar 

  • Streiff D, Lexer S, Gloessl K (1999) Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Mol Ecol 8:831–841

    Article  Google Scholar 

  • Torres CD, Puntieri J, Stecconi M (2012) Flower and seed production as affected by axis category and shoot size in two Patagonian Nothofagus species. Botany, in press

  • Valbuena-Carabana M, Gonzalez-Martinez SC, Sork VL, Collada C, Soto A, Goicoechea PG, Gil L (2005) Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea (Matts.) Liebl.) in central Spain. Heredity 95:457–465

    Article  PubMed  CAS  Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. University of Chicago Press, Chicago

    Google Scholar 

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Acknowledgments

We thank A. Martínez Meier and M. Millerón for field assistance, A. Martínez for nursery help, M. Millerón and C. Soliani for laboratory assistance, J.E. Gayone for computational help, and J.J. Robledo-Arnuncio and F. Austerlitz for helpful discussions on data analysis. We also thank a pair of anonymous reviewers for helpful commentary of the manuscript. The study was financed by the British Ecological Society Small Project Grant No. 2258, and PIP CONICET 5451. PES was funded by NJAES/USDA-17111 and NSF-DEB-0514956.

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  1. Grupo Genética Ecológica y Mejoramiento Forestal, INTA EEA Bariloche, Modesta Victoria 4450, CC 277, 8400, San Carlos de Bariloche, Rio Negro, Argentina

    Paula Marchelli & Leonardo A. Gallo

  2. Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

    Paula Marchelli

  3. Department of Ecology, Evolution and Natural Resources, School of Biological and Environmental Sciences, Rutgers University, New Brunswick, NJ, USA

    Peter E. Smouse

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  1. Paula Marchelli
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Correspondence to Paula Marchelli.

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Communicated by A. Kremer

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Marchelli, P., Smouse, P.E. & Gallo, L.A. Short-distance pollen dispersal for an outcrossed, wind-pollinated southern beech (Nothofagus nervosa (Phil.) Dim. et Mil.). Tree Genetics & Genomes 8, 1123–1134 (2012). https://doi.org/10.1007/s11295-012-0500-0

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