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Genetic differentiation between sun and shade habitats in populations of Lindera benzoin L.

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Population Ecology

Abstract

Differences in selection patterns among habitats can alter the distribution of genetic diversity even when this is estimated with neutral markers. For plants, light is an essential resource that can influence both abiotic and biotic components of habitat. We examined genetic differentiation between sun and shade habitats in Lindera benzoin L. (Spicebush), a perennial understory shrub. Genetic diversity of 127 plants from sun and shade habitats in two populations of L. benzoin was determined using 12 polymorphic microsatellite markers. We analyzed patterns of genetic diversity using analysis of molecular variance (AMOVA), and we assessed correlation between genetic and geographic distance using Mantel tests. We found (1) low levels of differentiation among populations (F ST = 0.028), (2) little evidence of genetic structure within populations due to isolation-by-distance, and (3) some evidence of habitat-based genetic differentiation. Specifically, the AMOVA showed a small (0.5%) but significant portion of overall variation could be explained by differences between habitats. The overall low levels of differentiation we saw were likely a result of extensive gene flow in this dioecious, bird-dispersed species.

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References

  • Balaguer L, Martinez-Ferri E, Valladares F, Perez-Corona ME, Baquedana FJ, Castillo FJ, Manrique E (2001) Population divergence in the plasticity of the response of Quercus coccifera to the light environment. Funct Ecol 15:124–135

    Article  Google Scholar 

  • Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol Ecol 11:771–783

    Article  CAS  PubMed  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165

    Article  PubMed  Google Scholar 

  • Bjørnstad ON, Iversen A, Hansen M (1995) The spatial structure of the gene pool of a viviparous population of Poa alpina—environmental controls and spatial constraints. Nord J Bot 15:347–354

    Article  Google Scholar 

  • Bockelmann AC, Reusch BH, Bijlsma R, Barker JP (2003) Habitat differentiation vs. isolation-by-distance: the genetic population structure of Elymus athericus in European salt marshes. Mol Ecol 12:505–515

    Article  CAS  PubMed  Google Scholar 

  • Bonnet E, Van de Peer Y (2002) zt: a software tool for simple and partial Mantel test. J Stat Softw 7:1–12

    Google Scholar 

  • Brothers TS, Spingarn A (1992) Forest fragmentation and alien plant invasion of central Indiana old-growth forests. Conserv Biol 6:91–100

    Article  Google Scholar 

  • Canham CD (1989) Different responses to gaps among shade-tolerant tree species. Ecology 70:548–550

    Article  Google Scholar 

  • Cardenasso ML, Pickett STA (2000) Linking forest edge structure to edge function: mediation of herbivore damage. J Ecol 88:31–44

    Article  Google Scholar 

  • Castellano S, Balletto E (2002) Is the partial Mantel test inadequate? Evolution 56:1871–1873

    PubMed  Google Scholar 

  • Chung MG, Chung MY, Oh GS, Epperson BK (2000) Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85:490–497

    Article  PubMed  Google Scholar 

  • Cipollini ML, Wallace-Senft DA, Whigham DF (1994) A model of patch dynamics, seed dispersal, and sex ratio in the dioecious shrub, Lindera benzoin. J Ecol 82:621–633

    Article  Google Scholar 

  • Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B 267:1149–1152

    Article  Google Scholar 

  • Dudley SA, Schmitt J (1995) Genetic differentiation in morphological responses to simulated foliage shade between populations of Impatiens capensis from open and woodland sites. Funct Ecol 9:655–666

    Article  Google Scholar 

  • Dupont YL (2002) Evolution of apomixis as a strategy of colonization in the dioecious species Lindera glauca (Lauraceae). Popul Ecol 44:293–297

    Article  Google Scholar 

  • Edwards MJ, Niesenbaum RA (2007) Eleven polymorphic microsatellite loci in Lindera benzoin, Lauraceae. Mol Ecol Notes 7:1302–1304

    Article  CAS  Google Scholar 

  • Estoup A, Rousset F, Michalakis Y, Cornuet JM, Adriamanga M, Guyomard R (1998) Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout Salmo trutta. Mol Ecol 7:339–353

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (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  Google Scholar 

  • Freville H, Justy F, Olivieri I (2001) Comparative allozyme and microsatellite population structure in a narrow endemic plant species, Centaurea corymbosa Pourret (Asteraceae). Mol Ecol 10:879–889

    Article  CAS  PubMed  Google Scholar 

  • Galeuchet DJ, Perret C, Fischer M (2005) Microsatellite variation and structure of 28 populations of the common wetland plant, Lychnis flos-cuculi L., in a fragmented landscape. Mol Ecol 14:991–1000

    Article  CAS  PubMed  Google Scholar 

  • Gauhl E (1976) Photosynthetic response to varying light intensity in ecotypes of Solanum dulcamara L. from shaded and exposed habitats. Oecologia 22:275–286

    Article  Google Scholar 

  • Gibson JP, Wheelwright NT (1995) Genetic structure in a population of tropical tree Ocotea tenera (Lauraceae): influence of avian seed dispersal. Oecologia 103:49–54

    Article  Google Scholar 

  • Godt MJW, Hamrick JL (1996) Allozyme diversity in the endangered shrub Lindera melissifolia (Lauraceae) and its widespread congener Lindera benzoin. Can J For Res 26:2080–2087

    Article  CAS  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat/html. Updated from Goudet (1995)

  • Goudet J, Raymond M, de-Meeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Harper KA, Macdonald SE, Burton PJ, Jiquan C, Brosofske KD, Saunders SC, Euskirchen ES, Roberts DAR, Jaiteh MS, Esseen P-A (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv Biol 19:768–782

    Article  Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their Interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Heywood JS (1991) Spatial analysis of genetic variation in plant populations. Annu Rev Ecol Syst 22:335–355

    Article  Google Scholar 

  • Hsiao JY, Lee SM (1999) Genetic diversity and microgeographic differentiation of Yushan cane (Yushania niitakayamensis; Poaceae) in Taiwan. Mol Ecol 8:263–270

    Article  Google Scholar 

  • Jonsson M, Bertilsson M, Ehrlen J, Lonn M (2008) Genetic divergence of climatically marginal populations of Vicia pisiformis on the Scandinavian Peninsula. Hereditas 145:1–8

    Article  PubMed  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Leclerc JC, Blaise S (1991) Photosynthetic and genetic differentiation in sun and shade populations of Holcus mollis L. Vegetatio 92:85–93

    Google Scholar 

  • Li Y-C, Röder MS, Fahima T, Kirzhner VM, Beiles A, Korol AB, Nevo E (2000a) Natural selection causing microsatellite divergence in wild emmer wheat at the ecologically variable microsite at Ammiad, Israel. Theor Appl Genet 100:985–999

    Article  Google Scholar 

  • Li Y-C, Fahima T, Peng JH, Röder MS, Kirzhner VM, Beiles A, Korol AB, Nevo E (2000b) Edaphic microsatellite DNA divergence in wild emmer wheat, Triticum dicoccoides, at a microsite: Tabigha, Israel. Theor Appl Genet 101:1029–1038

    Article  CAS  Google Scholar 

  • Li Y-C, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  CAS  PubMed  Google Scholar 

  • Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277

    Article  Google Scholar 

  • Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95

    Article  Google Scholar 

  • Malmborg PK, Willson MF (1988) Foraging ecology of avian frugivores and some consequences for seed dispersal in an Illinois woodlot. Condor 90:173–186

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    Google Scholar 

  • Matlack GR (1993) Microenvironment variation within and among forest edge sites in the eastern United States. Biol Conserv 66:185–194

    Article  Google Scholar 

  • Matlack GR (1994) Vegetation dynamics of the forest edge: trends in space and successional time. J Ecol 82:113–123

    Article  Google Scholar 

  • McEuen AB, Curran LM (2006) Plant recruitment bottlenecks in temperate forest fragments: seed limitation and insect herbivory. Plant Ecol 184:297–309

    Article  Google Scholar 

  • Medley KE (1996) Dieback in the native shrub, Lindera benzoin: a subtle effect of forest fragmentation. Ohio J Sci 96:76–80

    Google Scholar 

  • Meyer GA, Witmer MC (1998) Influence of seed processing by frugivorous birds on germination success of three North American shrubs. Am Midl Nat 140:129–139

    Article  Google Scholar 

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special references for microsatellite loci. Genetics 142:1061–1064

    CAS  PubMed  Google Scholar 

  • Murcia C (2000) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62

    Article  Google Scholar 

  • Muth NZ, Kluger EC, Levy JH, Edwards MJ, Niesenbaum RA (2008) Increased per capita herbivory in the shade: necessity, feedback or luxury consumption? Ecoscience 15:182–188

    Article  Google Scholar 

  • Nevo E, Behrav A, Meyer RC, Hackett CA, Forster BP, Russell JR, Powell W (2005) Genomic microsatellite adaptive divergence of wild barley by microclimatic stress in ‘Evolution Canyon’, Israel. Biol J Linn Soc 84:205–224

    Article  Google Scholar 

  • Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity 86:641–647

    Article  CAS  PubMed  Google Scholar 

  • Niesenbaum RA (1992a) The effects of light environment on herbivory and growth in the dioecious shrub Lindera benzoin (Lauraceae). Am Midl Nat 128:270–275

    Article  Google Scholar 

  • Niesenbaum RA (1992b) Sex ratio, components of reproduction, and pollen deposition in Lindera benzoin (Lauraceae). Am J Bot 79:495–500

    Article  Google Scholar 

  • Niesenbaum RA (1993) Light or pollen—seasonal limitations on female reproductive success in the understory shrub Lindera benzoin. J Ecol 81:315–323

    Article  Google Scholar 

  • Niesenbaum RA, Kluger EC (2006) When studying the effects of light on herbivory, should one consider temperature? The case of Epimecis hortaria F. (Lepidoptera: Geometridae) feeding on Lindera benzoin L. (Lauraceae). Environ Entomol 36:600–606

    Article  Google Scholar 

  • Nybom N (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Raufaste N, Rousset F (2001) Are partial Mantel tests adequate? Evolution 55:1703–1705

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60:696–710

    PubMed  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629

    Article  PubMed  Google Scholar 

  • Shure DJ, Phillips DL (1991) Patch size of forest openings and arthropod populations. Oecologia 86:325–334

    Article  Google Scholar 

  • Skoczylas DR, Muth NZ, Niesenbaum RA (2007) Contribution of insectivorous avifauna to top down control of Lindera benzoin herbivores at forest edge and interior habitats. Acta Oecol 32:337–342

    Article  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  CAS  PubMed  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed  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, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632

    Article  Google Scholar 

  • Turesson G (1922) The genotypical response of the plant species to the habitat. Hereditas 3:211–350

    Article  Google Scholar 

  • 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 4:535–538

    Article  CAS  Google Scholar 

  • Veres JS, Pickett STA (1982) Branching patterns of Lindera benzoin beneath gaps and closed canopies. New Phytol 91:767–772

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Whitmore TC (1989) Canopy gaps and the two major groups of forest trees. Ecology 70:536–538

    Article  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

  • Xiaohong Y, Qigang Y, Ming K, Hongwen H (2007) Microsatellite analysis reveals interpopulation differentiation and gene flow in the endangered tree Changiostyrax dolichocarpa (Styracaceae) with fragmented distribution in central China. New Phytol 176:472–480

    Article  Google Scholar 

  • Yeh FC, Yang R, Boyle T, Ye Z, Xiyan JM (1997) POPGENE, the user-friendly shareware for population genetic analysis. University of Alberta, Canada, Molecular Biology and Biotechnology Centre

  • Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418

    Article  Google Scholar 

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Acknowledgments

We thank our colleagues C. Ingersoll and G. Benjamin for their help with the experiment. We also thank G. Kolber M. Sones, E. Honan, and E. Tiedeken for their help with data collection. This material is based upon work performed at Muhlenberg College supported by the National Science Foundation under grant No. 0442049 to R. A. Niesenbaum.

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Correspondence to Emily Mooney.

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Mooney, E., Edwards, M. & Niesenbaum, R. Genetic differentiation between sun and shade habitats in populations of Lindera benzoin L.. Popul Ecol 52, 417–425 (2010). https://doi.org/10.1007/s10144-010-0197-6

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