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.
Similar content being viewed by others
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
Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol Ecol 11:771–783
Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165
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
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
Bonnet E, Van de Peer Y (2002) zt: a software tool for simple and partial Mantel test. J Stat Softw 7:1–12
Brothers TS, Spingarn A (1992) Forest fragmentation and alien plant invasion of central Indiana old-growth forests. Conserv Biol 6:91–100
Canham CD (1989) Different responses to gaps among shade-tolerant tree species. Ecology 70:548–550
Cardenasso ML, Pickett STA (2000) Linking forest edge structure to edge function: mediation of herbivore damage. J Ecol 88:31–44
Castellano S, Balletto E (2002) Is the partial Mantel test inadequate? Evolution 56:1871–1873
Chung MG, Chung MY, Oh GS, Epperson BK (2000) Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85:490–497
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
Cunningham SA (2000) Depressed pollination in habitat fragments causes low fruit set. Proc R Soc Lond B 267:1149–1152
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
Dupont YL (2002) Evolution of apomixis as a strategy of colonization in the dioecious species Lindera glauca (Lauraceae). Popul Ecol 44:293–297
Edwards MJ, Niesenbaum RA (2007) Eleven polymorphic microsatellite loci in Lindera benzoin, Lauraceae. Mol Ecol Notes 7:1302–1304
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
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
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
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
Gauhl E (1976) Photosynthetic response to varying light intensity in ecotypes of Solanum dulcamara L. from shaded and exposed habitats. Oecologia 22:275–286
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
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
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
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372
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
Hedrick PW (1999) Perspective: highly variable loci and their Interpretation in evolution and conservation. Evolution 53:313–318
Heywood JS (1991) Spatial analysis of genetic variation in plant populations. Annu Rev Ecol Syst 22:335–355
Hsiao JY, Lee SM (1999) Genetic diversity and microgeographic differentiation of Yushan cane (Yushania niitakayamensis; Poaceae) in Taiwan. Mol Ecol 8:263–270
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
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Leclerc JC, Blaise S (1991) Photosynthetic and genetic differentiation in sun and shade populations of Holcus mollis L. Vegetatio 92:85–93
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
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
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
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95
Malmborg PK, Willson MF (1988) Foraging ecology of avian frugivores and some consequences for seed dispersal in an Illinois woodlot. Condor 90:173–186
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Matlack GR (1993) Microenvironment variation within and among forest edge sites in the eastern United States. Biol Conserv 66:185–194
Matlack GR (1994) Vegetation dynamics of the forest edge: trends in space and successional time. J Ecol 82:113–123
McEuen AB, Curran LM (2006) Plant recruitment bottlenecks in temperate forest fragments: seed limitation and insect herbivory. Plant Ecol 184:297–309
Medley KE (1996) Dieback in the native shrub, Lindera benzoin: a subtle effect of forest fragmentation. Ohio J Sci 96:76–80
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
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
Murcia C (2000) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62
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
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
Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity 86:641–647
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
Niesenbaum RA (1992b) Sex ratio, components of reproduction, and pollen deposition in Lindera benzoin (Lauraceae). Am J Bot 79:495–500
Niesenbaum RA (1993) Light or pollen—seasonal limitations on female reproductive success in the understory shrub Lindera benzoin. J Ecol 81:315–323
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
Nybom N (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Peakall R, Smouse P (2006) GENALEX 6: genetic analysis in Excel. Population software for teaching and research. Mol Ecol Notes 6:288–295
Raufaste N, Rousset F (2001) Are partial Mantel tests adequate? Evolution 55:1703–1705
Raymond M, Rousset F (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60:696–710
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
Shure DJ, Phillips DL (1991) Patch size of forest openings and arthropod populations. Oecologia 86:325–334
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
Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632
Turesson G (1922) The genotypical response of the plant species to the habitat. Hereditas 3:211–350
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
Veres JS, Pickett STA (1982) Branching patterns of Lindera benzoin beneath gaps and closed canopies. New Phytol 91:767–772
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Whitmore TC (1989) Canopy gaps and the two major groups of forest trees. Ecology 70:536–538
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10144-010-0197-6