Skip to main content
SpringerLink
Log in

Impact of asymmetric male and female gamete dispersal on allelic diversity and spatial genetic structure in valley oak (Quercus lobata Née)

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

The distribution and abundance of genetic diversity in plant populations is initiated by sexually asymmetric propagule dispersal through pollen and seeds. Because these processes occur serially, it is not transparent how each contributes to subsequent patterns of genetic diversity. Using combined seedling/seed coat assay for naturally distributed seedlings of Quercus lobata Née, we extracted male and female gametic genotypes, and then assessed (wind-vectored) paternal and (gravity- and animal-vectored) maternal contributions to spatially distributed allelic diversity. We evaluated 200 naturally recruited seedlings from 4 open patches away from any adult canopies (denoted ‘open’), and 174 seedlings from 14 patches immediately beneath adult canopies (denoted ‘canopy’). The open patches included 19 % long distant dispersal events of >1 km while the canopy patches contained seedlings from one tree overhead. For each patch type, we partitioned average allelic diversity for six microsatellite loci for the whole study site (γ) into separate within-patch (α) and among-patch (β) components, translated into among-patch divergence (δ). We found that α-diversity resulting from seed dispersal was much less than that from pollen dispersal in both patch types, while total γ-diversity across the site was similar. Divergence (δ) among canopy patches was significantly greater than δ among open patches. We then evaluated spatial genetic autocorrelation (kinship) patterns for both open and canopy strata, separately for male and female gametes. Female gametes showed sharply declining kinship with increasing distance for canopy patches and modestly for open patches. In sharp contrast, male gametes from both patches showed only subtle decline of kinship, but seedlings still showed significant structure across patch types. On balance, sexual asymmetry in propagule dispersal shapes both the abundance and distribution of allelic diversity, with pollen dispersal promoting overall diversity but reducing spatial structure, but seed-dispersal reduces overall diversity and markedly increases spatial genetic structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    PubMed Central  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(4):937–954

    Article  PubMed  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(2):193–204. doi:10.1038/sj.hdy.6800983

    Article  CAS  PubMed  Google Scholar 

  • Chybicki IJ, Burczyk J (2010) Realized gene flow within mixed stands of Quercus robur L. and Q. petraea (Matt.) L. revealed at the stage of naturally established seedling. Mol Ecol 19(10):2137–2151. doi:10.1111/j.1365-294X.2010.04632.x

    Article  CAS  PubMed  Google Scholar 

  • Crawford TJ (1984) The estimation of neighborhood parameters for plant populations. Heredity 52:273–283

    Article  Google Scholar 

  • Darley-Hill S, Johnson WC (1981) Acorn dispersal by the blue jay (Cyanocitta cristata). Oecologia 50(2):231–232

    Article  Google Scholar 

  • Dutech C, Sork VL, Irwin AJ, Smouse PE, Davis FW (2005) Gene flow and fine-scale genetic structure in a wind-pollinated tree species Quercus lobata (Fagaceaee). Am J Bot 92(2):252–261

    Article  CAS  PubMed  Google Scholar 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259. doi:10.1038/hdy.1994.35

    Article  Google Scholar 

  • Garcia C, Grivet D (2011) Molecular insights into seed dispersal mutualisms driving plant population recruitment. Acta Oecol 37(6):632–640. doi:10.1016/J.Actao.04.009

    Article  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(9):1947–1955. doi:10.1111/j.1365-294X.2006.03126.x

    Article  CAS  PubMed  Google Scholar 

  • Gomez JM (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26(5):573–584

    Article  Google Scholar 

  • Grivet D, Smouse PE, Sork VL (2005) A novel approach to an old problem: tracking dispersed seeds. Mol Ecol 14(11):3585–3595

    Article  PubMed  Google Scholar 

  • Grivet D, Robledo-Arnuncio JJ, Smouse PE, Sork VL (2009) Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata, Née). Mol Ecol 18(19):3967–3979. doi:10.1111/j.1365-294X.2009.04326.x

    Article  PubMed  Google Scholar 

  • Hamilton MB, Miller JR (2002) Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure. Genetics 162(4):1897–1909

    PubMed Central  PubMed  Google Scholar 

  • Heuertz M, Vekemans X, Hausman JF, Palada M, Hardy OJ (2003) Estimating seed versus pollen dispersal from spatial genetic structure in the common ash. Mol Ecol 12(9):2483–2495. doi:10.1046/j.135-294X.2003.01923.x

    Article  CAS  PubMed  Google Scholar 

  • Heywood JS (1991) Spatial analysis of genetic-variation in plant populations. Annu Rev Ecol Syst 22:335–355. doi:10.1146/annurev.es.22.110191.002003

    Article  Google Scholar 

  • Holbrook KM, Smith TB, Hardesty BD (2002) Implications of long-distance movements of frugivorous rain forest hornbills. Ecography 25(6):745–749

    Article  Google Scholar 

  • Isagi Y, Saito D, Kawaguchi H, Tateno R, Watanabe S (2007) Effective pollen dispersal is enhanced by the genetic structure of an Aesculus turbinata population. J Ecol 95(5):983–990. doi:10.1111/j.1365-2745.2007.01272.x

    Article  Google Scholar 

  • Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88(10):2427–2439

    Article  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17(18):4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Article  PubMed  Google Scholar 

  • Jost L (2010) Independence of alpha and beta diversities. Ecology 91(7):1969–1974

    Article  PubMed  Google Scholar 

  • Jost L, DeVries P, Walla T, Greeney H, Chao A, Ricotta C (2010) Partitioning diversity for conservation analyses. Divers Distrib 16(1):65–76. doi:10.1111/j.1472-4642.2009.00626.x

    Article  Google Scholar 

  • Karubian J, Sork VL, Roorda T, Duraes R, Smith TB (2010) Destination-based seed dispersal homogenizes genetic structure of a tropical palm. Mol Ecol 19(8):1745–1753

    Article  PubMed  Google Scholar 

  • Koenig WD, McEntee JP, Walters EL (2008) Acorn harvesting by acorn woodpeckers: annual variation and comparison with genetic estimates. Evol Ecol Res 10:811–822

    Google Scholar 

  • Koenig WD, Krakauer AH, Monahan WB, Haydock J, Knops JMH, Carmen WJ (2009) Mast-producing trees and the geographical ecology of western scrub-jays. Ecography 32(4):561–570. doi:10.1111/j.1600-0587.2008.05617.x

    Article  Google Scholar 

  • Krauss SL, He T, Barrett LG, Lamont BB, Enright NJ, Miller BP, Hanley ME (2009) Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana. Heredity 102(3):274–285. doi:10.1038/hdy.2008.118

    Article  CAS  PubMed  Google Scholar 

  • Moran EV, Clark JS (2012) Between-site differences in the scale of dispersal and gene flow in red oak. PLoS One 7(5):e36492. doi:10.1371/journal.pone.0036492

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70(12):3321–3323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 12:3157–3164

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28(19):2537–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pluess AR, Sork VL, Dolan B, Davis FW, Grivet D, Merg K, Smouse PE (2009) Short distance pollen movement in a wind-pollinated tree, Quercus lobata (Fagaceae). For Ecol Manage 258(5):735–744. doi:10.1016/j.foreco.2009.05.014

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing

  • Ravigne V, Olivieri I, Gonzalez-Martinez SC, Rousset F (2006) Selective interactions between short-distance pollen and seed dispersal in self-compatible species. Evolution 60(11):2257–2271. doi:10.1554/05-352.1

    Article  PubMed  Google Scholar 

  • Rousset F (2004) Genetic structure and selection in subdivided populations. Princeton University Press, Princeton

    Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytol 188(2):333–353

    Article  PubMed  Google Scholar 

  • Scofield DG (2015a) diversityDispersal: analyse individual and genetic diversity of dispersal processes in biological populations. R package version 0.9.9000. https://github.com/douglasgscofield/diversityDispersal

  • Scofield DG (2015b) readGenalex: read and manipulate GenAlEx-format genotype files. R package version 0.4.1. http://CRAN.R-project.org/package=readGenalex

  • Scofield DG, Sork VL, Smouse PE (2010) Influence of acorn woodpecker social behaviour on transport of coast live oak (Quercus agrifolia) acorns in a southern California oak savanna. J Ecol 98(3):561–572

    Article  Google Scholar 

  • Scofield DG, Alfaro VR, Sork VL, Grivet D, Martinez E, Papp J, Smouse PE (2011) Foraging patterns of acorn woodpeckers (Melanerpes formicivorus) on valley oak (Quercus lobata Née) in two California oak savanna-woodlands. Oecologia 166(1):187–196

    Article  PubMed Central  PubMed  Google Scholar 

  • Scofield DG, Smouse PE, Karubian J, Sork VL (2012) Use of Alpha, Beta, and Gamma diversity measures to characterize seed dispersal by animals. Am Nat 180(6):719–732. doi:10.1086/668202

    Article  PubMed  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

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

    Article  PubMed  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(2):260–271

    Article  CAS  PubMed  Google Scholar 

  • Smouse PE, Peakall R, Gonzales E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17(14):3389–3400

    Article  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(2):250–259

    Article  PubMed  Google Scholar 

  • Snedecor GW, Cochran WG (1989) Statistical methods, 8 ed. Iowa State University Press

  • Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landsc Ecol 21(6):821–836. doi:10.1007/s10980-005-5415-9

    Article  Google Scholar 

  • Sork V, Dyer R, Davis F, Smouse P (2002a) Mating system in California Valley oak, Quercus lobata Neé. In: Standiford RB, McCreary D, Purcell KL (eds) Proceedings of the fifth symposium on Oak Woodlands: Oaks in California’s changing landscape. 2001 October 22–25; San Diego, CA, Gen. Tech. Rep. PSW-GTR-184. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA, pp 427–444

  • Sork VL, Davis FW, Smouse PE, Apsit VJ, Dyer RJ, Fernandez-M JF, Kuhn B (2002b) Pollen movement in declining populations of California Valley oak, Quercus lobata: where have all the fathers gone? Mol Ecol 11(9):1657–1668

    Article  CAS  PubMed  Google Scholar 

  • Thompson PT, Smouse PE, Scofield DG, Sork VL (2014) What seeds tell us about bird movement: a multi-year analysis of Acorn Woodpecker foraging patterns on two oak species. Mov Ecol. doi:10.1186/2051-3933-2-12

    PubMed Central  PubMed  Google Scholar 

  • Tuomisto H (2010) A consistent terminology for quantifying species diversity? Yes, it does exist. Oecologia 164(4):853–860. doi:10.1007/s00442-010-1812-0

    Article  PubMed  Google Scholar 

  • Tyler CM, Kuhn B, Davis FW (2006) Demography and recruitment limitations of three oak species in California. Q Rev Biol 81(2):127–152

    Article  PubMed  Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13(4):921–935

    Article  CAS  PubMed  Google Scholar 

  • Wenny DG (2001) Advantages of seed dispersal: a re-evaluation of directed dispersal. Evol Ecol Res 3(1):51–74

    Google Scholar 

  • Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30(3):279–338

    Article  Google Scholar 

  • Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21(2/3):213–251

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wright S (1946) Isolation by distance under diverse systems of mating. Genetics 31:39–59

    PubMed Central  Google Scholar 

  • Zavaleta ES, Hulvey KB, Fulfrost B (2007) Regional patterns of recruitment success and failure in two endemic California oaks. Divers Distrib 13(6):735–745

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank F. Davis (UCSB) for our early collaboration. The fieldwork was performed at the University of California Natural Reserve System Sedgwick Reserve administered by the UC Santa Barbara. We thank M. Williams, K. McCurdy, A. Lentz, and the staff at the Sedgwick Reserve for logistical support over the years. We thank F. Austerlitz and J. J. Arnuncio for intellectual stimulation. For technical assistance in genotyping and scoring genotypes of difficult tissue, we are grateful to C. Winder of the Sork lab and J. Papp and U. Dandekar of the UCLA Genotyping Core facility. We thank members of the Sork lab for comments on earlier versions of this manuscript. The research and V.L.S, D.G., D.G.S. were supported by NSF-DEB-0514956 and NSF-DEB-0089445; P.E.S. was supported by NSF-DEB-0514956 and USDA/NJAES-17111 and -17160.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Los Angeles, CA, 90095-7239, USA

    Victoria L. Sork & Douglas G. Scofield

  2. Institute of the Environment and Sustainability, University of California, Los Angeles, Los Angeles, CA, USA

    Victoria L. Sork

  3. Department of Ecology, Evolution and Natural Resources, Rutgers University, New Brunswick, NJ, 08901-8551, USA

    Peter E. Smouse

  4. Department of Forest Ecology and Genetics, Center of Forest Research, CIFOR-National Institute for Agriculture and Food Research and Technology, Madrid, Spain

    Delphine Grivet

  5. Department of Ecology and Genetics, Evolutionary Biology Centre, Uppsala University, 75236, Uppsala, Sweden

    Douglas G. Scofield

Authors
  1. Victoria L. Sork
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter E. Smouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Delphine Grivet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Douglas G. Scofield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victoria L. Sork.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sork, V.L., Smouse, P.E., Grivet, D. et al. Impact of asymmetric male and female gamete dispersal on allelic diversity and spatial genetic structure in valley oak (Quercus lobata Née). Evol Ecol 29, 927–945 (2015). https://doi.org/10.1007/s10682-015-9769-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-015-9769-4

Keywords

Search

Navigation