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Pollination graphs: quantifying pollen pool covariance networks and the influence of intervening landscape on genetic connectivity in the North American understory tree, Cornus florida L.

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Abstract

The manner by which pollinators move across a landscape and their resulting preferences and/or avoidances of travel through particular habitat types can have a significant impact on plant population genetic structure and population-level connectivity. We examined the spatial genetic structure of the understory tree Cornus florida (Cornaceae) adults (N Adults = 452) and offspring (N Offspring = 736) across two mating events to determine the extent to which pollen pool genetic covariance is influenced by intervening forest architecture. Resident adults showed no spatial partitioning but genotypes were positively autocorrelated up to a distance of 35 m suggesting a pattern of restricted seed dispersal. In the offspring, selfing rates were small (sm = 0.035) whereas both biparental inbreeding (s b;open canopy = 0.16, s b;closed canopy = 0.11) and correlated paternity (r p;open canopy = 0.21, r p;closed canopy = 0.07) were significantly influenced by primary canopy opening above individual mothers. The spatial distribution of genetic covariance in pollen pool composition was quantified for each reproductive event using Pollination Graphs, a network method based upon multivariate conditional genetic covariance. The georeferenced graph topology revealed a significant positive relationship between genetic covariance and pollinator movement through C. florida canopies, a negative relationship with open primary canopy (e.g., roads under open canopies and fields with no primary canopy), and no relationship with either conifer or mixed hardwood canopy species cover. These results suggest that both resident genetic structure within stands and genetic connectivity between sites in C. florida populations are influenced by spatial heterogeneity of mating individuals and quality of intervening canopy cover.

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References

  • Albert R, Barabasi AL (2002) Statistical mechanics of complex networks. Rev Modern Phys 74:47–97

    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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Barabási AL, Albert R (1999) Emergence of scaling in random networks. Science 286:251–262

    Google Scholar 

  • Cabe PR, Liles JS (2002) Dinucleotide microsatellite loci isolated from flowering dogwood (Cornus florida L.). Mol Ecol Notes 2:150–152

    CAS  Google Scholar 

  • Cain ML, Damman H, Muir A (1998) Seed dispersal and the holocene migration of woodland herbs. Ecol Monogr 68:325–347

    Google Scholar 

  • Carlquist S (1967) The biota of long-distance dispersal. V: plant dispersal to Pacific islands. Bull Torrey Botanical Club 94:129–162

    Google Scholar 

  • Carr D (2010) Canopy disturbance and reproduction in Cornus florida L. Masters Thesis, Virginia Commonwealth University. http://hdl.handle.net/10156/3078

  • Craft KJ, Ashley MV (2010) Pollen-mediated gene flow in isolated and continuous stands of bur oak, Quercus macrocarpa (Fagaceae). Am J Bot 97:1999–2006

    PubMed  Google Scholar 

  • Cushman SA, Lewis JS (2010) Movement behavior explains genetic differentiation in American black bears. Landscape Ecol 25:1613–1625

    Google Scholar 

  • Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499

    PubMed  Google Scholar 

  • de Moraes MLT, Sebbenn AM (2011) Pollen dispersal between isolated trees in the Brazilian Savannah: a case study of the neotropical tree Hymeneae stigonocarpa. Biotropica 43:192–199

    Google Scholar 

  • Devaux C, Lavigne C, Austerlitz F, Klein EK (2007) Modeling and estimating pollen movement in oilseed rape (Brassica napus) at the landscape scale using genetic markers. Mol Ecol 16:487–499

    PubMed  CAS  Google Scholar 

  • Dyer RJ (2007) The evolution of genetic topologies. Theor Popul Biol 71:71–79

    PubMed  Google Scholar 

  • Dyer RJ (2009) GeneticStudio: a suite of programs for the spatial analysis of genetic marker data. Mol Ecol Resour 9:110–113

    PubMed  Google Scholar 

  • Dyer RJ, Nason JD (2004) Population Graphs: the graph theoretic shape of genetic structure. Mol Ecol 13:1713–1727

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dyer RJ, Westfall RD, Sork VL, Smouse PE (2004) Two-generation analysis of pollen flow across a landscape V: a stepwise approach for extracting factors contributing to pollen structure. Heredity 92:204–211

    PubMed  CAS  Google Scholar 

  • Dyer RJ, Nason JD, Garrick RC (2010) Landscape modeling of gene flow: improved power using conditional genetic distance derived from population networks. Mol Ecol 19:3746–3759

    PubMed  Google Scholar 

  • Ellstrand NC, Marshall DL (1985) Interpopulation gene flow by ollen in wild radish, Raphanus sativus. Am Nat 126:606–610

    Google Scholar 

  • Ennos RA (1994) Estimating relative rates of pollen and seed migration among plant populations. Heredity 72:250–259

    Google Scholar 

  • Eriksson O (1996) Regional dynamics of plants: a review of evidence for remnant source-sink and metapopulations. Oikos 77:248–258

    Google Scholar 

  • Fagan WF, Cantrell RS, Cosner C (1999) How habitat edges change species interactions. Am Nat 153:165–182

    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

    PubMed  Google Scholar 

  • Fortuna MA, Garcia C, Guimaraes PR, Bascompte J (2008) Spatial mating networks in insect-pollinated plants. Ecol Lett 11:490–498

    PubMed  Google Scholar 

  • Fuchs EJ, Hamrick JL (2011) Mating system and pollen flow between remnant populations of the endangered tropical tree, Guaiacum sanctum (Zygophyllaceae). Conserv Genet 12:175–185

    Google Scholar 

  • Gardiakos VA (2009) Pollen-mediated gene movement in flowering dogwood, Cornus florida L. Masters Thesis, Virginia Commonwealth University

  • Geffen E, Anderson MJ, Wayne RK (2004) Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13:2481–2490

    PubMed  CAS  Google Scholar 

  • Grass Development Team (2008) Geographic Resources Analysis Support System (GRASS) Software. Open source geospatial foundation project. http://grass.osgeo.org

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

    PubMed  CAS  Google Scholar 

  • Higgins SI, Richardson DM (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. Am Nat 153:464–475

    Google Scholar 

  • Holzhauer SIJ, Ekschmitt K, Sander AC, Dauber J, Wolters V (2006) Effects of historic landscape change on the genetic structure of the bush-cricket. Landscape Ecol 21:891–899

    Google Scholar 

  • Husband BC, Barrett SCH (1996) A metapopulation perspective in plant population biology. J Ecol 84:461–469

    Google Scholar 

  • Iwaizumi MG, Takahashi M, Watanabe A, Ubukata M (2010) Simultaneous evaluation of paternal and maternal immigrant gene flow and the implications for the overall genetic composition of Pinus densiflora dispersed seeds. J Hered 101:144–153

    PubMed  CAS  Google Scholar 

  • Keller EF (2005) Revisiting ‘scale-free’ networks. BioEssays 27:1060–1068

    PubMed  Google Scholar 

  • Machado ICS, Sazima I, Sazima M (1998) Bat pollination of the terrestrial herb Irlbachia alata (Gentianaceae) in northeastern Brazil. Plant Syst Evol 209:231–237

    Google Scholar 

  • Manel S, Schwrtz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Google Scholar 

  • Mayor AJ, Grant JF, Windham MT, Trigiano RN (1999) Insect visitors to flowers of flowering dogwood, Cornus florida L., in eastern Tennessee: potential pollinators. South Nurseries Assoc Res Conf 44:192–196

    Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    PubMed  Google Scholar 

  • Meagher TR, Vassiliadis C (2003) Spatial geometry determines gene flow in plant populations. In: Hails R, Beringer J, Godfray HC (eds) Genes in environment: 15th special symposium of the British Ecological Society. British Ecological Society, London

    Google Scholar 

  • Moran EV, Clark JS (2011) Estimating seed and pollen movement in a monoecious plant: a hierarchical Bayesian approach integrating genetic and ecological data. Mol Ecol 20:1248–1262

    PubMed  Google Scholar 

  • Murphy MA, Dezzani R, Pilliod DS, Storfer A (2010) Landscape genetics of high mountain frog metapopulations. Mol Ecol 19:2624–2649

    Google Scholar 

  • Nielsen R, Mattila DK, Clapman PJ, Palsbøll PJ (2001) Statistical approaches to paternity analysis in natural populations and applications to the North Atlantic Humpback Whale. Genetics 157:1673–1682

    PubMed  CAS  Google Scholar 

  • Nigel JE (1997) A comparison of alternative strategies for estimating gene flow from markers. Ann Rev Ecol Syst 28:105–128

    Google Scholar 

  • Oddou-Muratorio S, Bontemps A, Klein EK, Chybicki I, 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

    Google Scholar 

  • Ohashi K, Thomson JD (2009) Trapline foraging by pollinators: its ontogeny, economics, and possible consequences for plants. Ann Bot 103:1365–1378

    PubMed  Google Scholar 

  • Ohashi K, Thomson JD, D’souza D (2007) Trapline foraging by bumble bees: IV. Optimization of route in the absence of competition. Behav Ecol 18:1–11

    Google Scholar 

  • Ohashi K, Alison L, Thomson JD (2008) Trapline foraging by bumble bees: V. Effects of experience and priority on competitive performance. Behav Ecol 19:936–948

    Google Scholar 

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

    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

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Radford AE, Ahles HE, Bell CR (1968) Manual of the vascular plants of the Carolinas. The University of North Carolina Press, Chapel Hill

    Google Scholar 

  • Rayfield B, Fortin MJ, Fall A (2010) The sensitivity of least-cost habitat graphs to relative cost surface values. Landscape Ecol 25:519–532

    Google Scholar 

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

    PubMed  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 94:12–22

    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

    PubMed  CAS  Google Scholar 

  • Schnabel AR, Nason JD, Hamrick JL (1998) Understanding the population genetic structure of Gleditsia triacanthos L.: seed dispersal and variation in female reproductive success. Mol Ecol 7:819–832

    Google Scholar 

  • Shaw R (2009) Shrinking the Janzen-Connell Doughnut: Consequences of an invasive multiplier (Microstegium vimineum) on the mid-canopy in a mixed pine-oak forest. Masters Thesis, Virginia Commonwealth University. http://hdl.handle.net/10156/2491

  • Skellam JG (1951) Random dispersal in theoretical populations. Biometrika 38:196–218

    PubMed  CAS  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Ann Rev Ecol Syst 16:393–430

    Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sorensen AE (1986) Seed dispersal by adhesion. Ann Rev Ecol Syst 17:443–463

    Google Scholar 

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

    Google Scholar 

  • Sork VL, Nason JD, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224

    PubMed  Google Scholar 

  • Sork VL, Davis FW, Smouse PE, Apsit VJ, Dyer RJ, Fernandez-Manjarres 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

    PubMed  CAS  Google Scholar 

  • Sork VL, Smouse PE, Apsit VJ, Dyer RJ, Westfall RD (2004) A two-generation analysis of pollen pool genetic structure in flowering dogwood, Cornus florida (Cornaeceae), in the Missouri Ozarks. Am J Bot 92:262–271

    Google Scholar 

  • Thomson JD, Peterson SC, Harder LD (1987) Response of traplining bumble bees to competition experiments: shifts in feeding location and efficiency. Oecologia 71:295–300

    Google Scholar 

  • Waddington CH (1957) The strategy of the genes. George Allen and Unwin Publishers, Crows Nest

    Google Scholar 

  • Wang IJ, Savage WK, Bradley-Shaffer H (2009) Landscape genetics and least-cost path analysis reveal unexpected dispersal routes in the California tiger salamander (Amybstoma californiense). Mol Ecol 18:1365–1374

    PubMed  Google Scholar 

  • Wang J, Kang M, Gao PX, Huang HW (2010) Contemporary pollen flow and mating patterns of a subtropical canopy tree Eurycorymbus cavaleriei in a fragmented agricultural landscape. For Ecol Manag 260:2180–2188

    Google Scholar 

  • White GM, Boshier DH, Powell W (2002) Increased pollen flow contracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Nat Acad Sci (USA) 99:2038–2042

    CAS  Google Scholar 

  • Young JA, Young CG (1994) Seeds of woody plants of North America. Dioscorides Press, Portland

    Google Scholar 

  • Young AG, Merriam HG, Warwick SI (1993) The effects of forest fragmentation on genetic variation in Acer saccharum Marsh (sugar maple) populations. Heredity 71:277–289

    Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the National Science Foundation (DEB-0640803) to RJD and DMC. Both VAG and CAM were supported in part by graduate research grants from the Rice Center for Environmental Studies. The authors would also like to thank Jennifer Cimminelli, Will Shuart, and the Center for Environmental Science at Virginia Commonwealth University for assistance with spatial modeling analyses. This manuscript is the Virginia Commonwealth University Rice Center Contribution #18.

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Correspondence to Rodney J. Dyer.

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Dyer, R.J., Chan, D.M., Gardiakos, V.A. et al. Pollination graphs: quantifying pollen pool covariance networks and the influence of intervening landscape on genetic connectivity in the North American understory tree, Cornus florida L.. Landscape Ecol 27, 239–251 (2012). https://doi.org/10.1007/s10980-011-9696-x

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