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Genetic diversity and spatial genetic structure of Pinus strobus (Pinaceae) across an island landscape inferred from allozyme and cpDNA markers

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Abstract

The Beaver Island Archipelago (BIA) provides a model system to address the impact of long-term isolation on genetic diversity and gene flow. Low lake levels are assumed to have caused the BIA to be attached to mainland Michigan for at least 4000 years (10000 yr B.P.- 6000 yr B.P.), eventually, rising lake levels would have kept the islands isolated since 6000 yr B.P. If the island populations of a plant species in the BIA were indeed once continuous with the mainland of Michigan, then we would expect similar levels of genetic diversity in populations of such a species on the islands vs. the mainland. We compared levels of allozyme genetic diversity of 20 plots of Pinus strobus in the BIA with two mainland populations in northern Michigan. In addition, if pollen is a primary agent of gene flow across islands, a low degree of allozyme differentiation among the island populations of P. strobus in the BIA would be evident. Furthermore, since seed dispersal is more limited than pollen dispersal in P. strobus, a more pronounced spatial genetic structure (SGS) is expected in allozymes than in cpDNA markers. To gain insights on the pattern of seed and pollen dispersal among the 20 plots, we further analyzed spatial autocorrelation using Moran's I-statistics for both data sets [biparentally inherited, allozymes and paternally inherited, cpDNA microsatellites (cpDNA SSR)]. We found a similar level of allozyme variability in both the BIA (mean H e = 0.080) and the two mainland populations (mean H e = 0.078). As predicted, we observed a low but significant degree of genetic divergence among populations for allozymes (mean F ST = 0.033 across 20 plots). Our allozyme-based SGS analysis revealed significant evidence of SGS (i.e. isolation-by-distance; slope β = −0.194 from regression analysis of observed averaged Moran's I values against the logarithm of the upper bound of six distance classes). In contrast, little evidence of SGS was found in cpDNA SSR data across the BIA (β = 0.013). These results suggest that although gene flow via seed dispersal is somewhat limited, pollen flow has been sufficient to maintain genetic diversity and prevent differentiation across the island landscape over several thousand years of isolation.

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References

  • J. Beaulieu J. P. Simon (1994) ArticleTitleGenetic structure and variability in Pinus strobus in Quebec Canad. J. For. Res. 24 1726–1733

    Google Scholar 

  • J. Beaulieu J. P. Simon (1995) ArticleTitleMating system in natural populations of eastern white pine in Quebec Canad. J. For. Res. 25 1697–1703

    Google Scholar 

  • Cheliak W. M., Pitel J. P. (1984) Technique for starch gel electrophoresis of enzyme from forest tree species. Information report PI-X-42. Petawawa National Forestry Institute, Chalk River, Ontario, Canada.

  • M. G. Chung (1996) ArticleTitleSpatial genetic structure among Korean populations of Hosta minor and H. capitata (Liliaceae) Bot. Bull. Acad. Sin. 37 25–30

    Google Scholar 

  • M. G. Chung S. S. Kang (1994) ArticleTitleGenetic variation and population structure in Korean populations of Eurya japonica (Theaceae) Amer. J. Bot. 81 1077–1082 Occurrence Handle10.2307/2445303

    Article  Google Scholar 

  • M. Y. Chung J. D. Nason M. G. Chung (2005) ArticleTitlePatterns of hybridization and population genetic structure in the terrestrial orchids Liparis kumokiri and Liparis makinoana (Orchidaceae) in sympatric populations Molec. Ecol. 14 4389–4402 Occurrence Handle1:CAS:528:DC%2BD28XhvFagsw%3D%3D Occurrence Handle10.1111/j.1365-294X.2005.02738.x

    Article  CAS  Google Scholar 

  • A. D. Cliff J. K. Ord (1981) Spatial processes: methods and applications Pion London, UK

    Google Scholar 

  • Critchfield W. B. (1980) Genetics of lodgepole pine. USDA Forest Service Research paper WO-37.

  • A. Doligez H. I. Joly (1997) ArticleTitleGenetic diversity and spatial structure within a natural stand of a tropical forest tree species, Carapa procera (Meliaceae), French Guiana Heredity 79 72–82 Occurrence Handle10.1038/sj.hdy.6881590

    Article  Google Scholar 

  • J. Dong D. B. Wagner (1994) ArticleTitlePaternally inherited chloroplast polymorphism in Pinus: estimation of diversity and population subdivision, and tests of disequilibrium with a maternally inherited mitochondrial polymorphism Genetics 136 1187–1194 Occurrence Handle8005423 Occurrence Handle1:STN:280:DyaK2c3nsVSiuw%3D%3D

    PubMed  CAS  Google Scholar 

  • R. T. Eckert R. J. Joly D. B. Neale (1981) ArticleTitleGenetics of isozyme variants and linkage relationships among allozyme loci in 35 eastern white pine clones Canad. J. For. Res. 11 573–579 Occurrence Handle1:CAS:528:DyaL3MXlvVCjt7w%3D

    CAS  Google Scholar 

  • B. K. Epperson (1990) ArticleTitleSpatial autocorrelation of genotypes under directional selection Genetics 124 757–771 Occurrence Handle2311920 Occurrence Handle1:STN:280:DyaK3c7osFWmsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • B. K. Epperson (2003) Geographical genetics Princeton University Press Princeton, New Jersey

    Google Scholar 

  • B. K. Epperson (2005) ArticleTitleMutation at high rates reduces spatial structure within populations Molec. Ecol. 14 703–710 Occurrence Handle10.1111/j.1365-294X.2005.02429.x Occurrence Handle1:CAS:528:DC%2BD2MXjtVGitr0%3D

    Article  CAS  Google Scholar 

  • B. K. Epperson M. G. Chung (2001) ArticleTitleSpatial genetic structure of allozyme polymorphisms within populations of Pinus strobus (Pinaceae) Amer. J. Bot. 88 1006–1010 Occurrence Handle10.2307/2657081 Occurrence Handle1:CAS:528:DC%2BD3MXltV2qu7w%3D

    Article  CAS  Google Scholar 

  • W. J. Ewens (1979) Mathematical population genetics Springer New York, New York

    Google Scholar 

  • C. B. Fenster X. Vekemans O. J. Hardy (2003) ArticleTitleQuantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae) Evolution 57 995–1007 Occurrence Handle12836818 Occurrence Handle10.1554/0014-3820(2003)057[0995:QGFFSG]2.0.CO;2

    Article  PubMed  Google Scholar 

  • J. P. Gibson J. L. Hamrick (1991) ArticleTitleGenetic diversity and structure in Pinus pungens (table mountain pine) populations. Canad J. For. Res. 21 635–642

    Google Scholar 

  • Goudet J. (2002) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3.2. Computer program and documentation distributed by the author, website: http://www.unil.ch/izea/softwares/fstat.html.

  • J. L. Hamrick M. J. W. Godt (1989) Allozyme diversity in plant species A. H. D. Brown M. T. Clegg A. L. Kahler B. S. Weir (Eds) Plant population genetics, breeding and genetic resources Sinauer Sunderland 43–63

    Google Scholar 

  • Hansel A., Mickelson D., Schneider A., Larson D. C. (1985) Late Wisconsin and Holocene history of the Lake Michigan basin. Geological Association of Canada Special Paper 30.

  • L. D. Harris (1984) The fragmented forest: island biogeography theory and the preservation of biotic diversity University of Chicago Press Chicago

    Google Scholar 

  • Hatt R., Tyne J., Stuart L., Pope C., Grobman A. (1950) Island life: a study of the land vertebrates of the islands of eastern Lake Michigan. Cranbook Institute of Science Bulletin 27.

  • C. H. Haufler (1985) ArticleTitleEnzyme variability and modes of evolution in Bomeria (Pteridaceae) Syst. Bot. 10 92–104 Occurrence Handle10.2307/2418438

    Article  Google Scholar 

  • R. D. Hiebert J. L. Hamrick (1983) ArticleTitlePatterns and levels of genetic variation in great basin bristlecone pine Pinus longaeva Evolution 37 301–310 Occurrence Handle10.2307/2408339

    Article  Google Scholar 

  • T. Y. James D. Porter J. L. Hamrick R. Vilgalys (1999) ArticleTitleEvidence for limited intercontinental gene flow in the cosmopolitan mushroom, Schizophyllum commune Evolution 53 1665–1677 Occurrence Handle10.2307/2640430 Occurrence Handle1:CAS:528:DC%2BD3cXmtV2lsA%3D%3D

    Article  CAS  Google Scholar 

  • S. Kalisz J. D. Nason F. M. Hanzawa S. J. Tonsor (2001) ArticleTitleSpatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history and selection Evolution 55 1560–1568 Occurrence Handle11580015 Occurrence Handle10.1554/0014-3820(2001)055[1560:SPGSIT]2.0.CO;2 Occurrence Handle1:STN:280:DC%2BD3MrjtlaktQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • S. S. Kang M. G. Chung (1997) ArticleTitleGenetic variation and population structure in Korean endemic species: IV. Hemerocallis hakuunensis (Liliaceae) J. Pl. Res. 110 209–217 Occurrence Handle10.1007/BF02509309

    Article  Google Scholar 

  • Kapp R. O. (1999) Michigan Late Pleistocene, Holocene, and presettlement vegetation and climate. In: Halsey J. R. (ed.) Retrieving Michigan's buried past: The Archaeology of the Great Lakes State. Cranbrook Institute of Science Bulletin 64, Bloomfield Hills, Michigan, pp. 31–58.

  • T. J. Karamanski (1989) Deep woods frontier. A history of logging in northern Michigan Wayne State University Detroit, Michigan

    Google Scholar 

  • R. G. Latta J. B. Mitton (1997) ArticleTitleA comparison of population differentiation across four classes of gene marker in limber pine (Pinus flexilis James) Genetics 146 1153–1163 Occurrence Handle9215916 Occurrence Handle1:CAS:528:DyaK2sXmsVarurk%3D

    PubMed  CAS  Google Scholar 

  • R. G. Latta Y. B. Linhart D. Fleck M. Elliot (1988) ArticleTitleDirect and indirect estimates of seed vs pollen movement within a population of ponderosa pine Evolution 52 61–67 Occurrence Handle10.2307/2410920

    Article  Google Scholar 

  • C. F. M. Lewis T. C. Moore SuffixJr. D. K. Rea D. L. Dettman A. M. Smith L. A. Mayer (1994) ArticleTitleLakes of the Huron Basin: their record of runoff from the Laurentide ice sheet Quaternary Science Reviews 13 891–922 Occurrence Handle10.1016/0277-3791(94)90008-6

    Article  Google Scholar 

  • Lewis P. O., Zaykin D. (2001) Genetic data analysis: computer program for the analysis of allelic data, version 1.0[d16c]. Computer program and documentation distributed by the author, website: http://lewis.eeb.uconn.edu/lewishome/software.html.

  • Little E. L., Jr. (1971) Atlas of United States trees. Vol. 1. Conifers and important hardwoods. USDA Forest Service Miscellaneous Publications 1146. Washington, D. C. USA.

  • S. Mariette D. Chagné C. Lézier P. Pastuszka A. Raffin C. Plomion (2001) ArticleTitleGenetic diversity within and among Pinus pinaster populations: comparison between AFLP and microsatellite markers Heredity 86 469–479 Occurrence Handle11520347 Occurrence Handle10.1046/j.1365-2540.2001.00852.x Occurrence Handle1:CAS:528:DC%2BD3MXmsVyjsLc%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Marquardt B. K. Epperson (2004) ArticleTitleSpatial and population genetic structure of microsatellites in white pine Molec. Ecol. 13 3305–3315 Occurrence Handle10.1111/j.1365-294X.2004.02341.x Occurrence Handle1:CAS:528:DC%2BD2cXhtVWkurvL

    Article  CAS  Google Scholar 

  • J. B. Mitton Y. B. Linhart K. B. Sturgeon J. L. Hamrick (1979) ArticleTitleAllozyme polymorphisms detected in mature needle tissue of ponderosa pine J. Heredity 70 86–89 Occurrence Handle1:CAS:528:DyaE1MXkvVOnur0%3D

    CAS  Google Scholar 

  • D. B. Neale R. R. Sederoff (1989) ArticleTitlePaternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine Theor. Appl. Genet. 77 212–216 Occurrence Handle10.1007/BF00266189

    Article  Google Scholar 

  • S. Oddou-Muratoria B. Demesure-Musch R. Pélissier P.-H. Gouyon (2004) ArticleTitleImpacts of gene flow and logging history on the local genetic structure of a scattered tree species, Sorbus torminalis L Crantz. Molec. Ecol. 13 3689–3702 Occurrence Handle10.1111/j.1365-294X.2004.02373.x

    Article  Google Scholar 

  • N. J. Ouborg Y. Piquet J. M. Groenendael ParticleVan (1999) ArticleTitlePopulation genetics, molecular markers and the study of dispersal in plants J. Ecol. 87 551–568 Occurrence Handle10.1046/j.1365-2745.1999.00389.x

    Article  Google Scholar 

  • G. Pielou (1991) After the Ice Age, the return of life to glaciated North America University of Chicago Press Chicago, Ill

    Google Scholar 

  • R. J. Preston (1989) North American trees EditionNumber4 Iowa State University Press Ames, Iowa

    Google Scholar 

  • O. P. Rajora L. Deverno A. Mosseler D. J. Innes (1998) ArticleTitleGenetic diversity and population structure of disjunct Newfoundland and central Ontario populations of eastern white pine (Pinus strobus) Canad. J. Bot. 76 500–508 Occurrence Handle10.1139/cjb-76-3-500

    Article  Google Scholar 

  • R. I. Righter (1939) ArticleTitleEarly flower production among the pines J. Forestry 37 935–938

    Google Scholar 

  • S. K. Robinson F. R. Thompson T. M. Dovovan D. R. Whitehead J. Faaborg (1995) ArticleTitleRegional forest fragmentation and the nesting success of migratory birds Science 267 1987–1990 Occurrence Handle10.1126/science.267.5206.1987 Occurrence Handle1:CAS:528:DyaK2MXkslOktbY%3D Occurrence Handle17770113

    Article  CAS  PubMed  Google Scholar 

  • F. Rousset (1997) ArticleTitleGenetic differentiation and estimation of gene flow from F-statistics under isolation by distance Genetics 145 1219–1228 Occurrence Handle9093870 Occurrence Handle1:STN:280:DyaK2s3kslOntQ%3D%3D

    PubMed  CAS  Google Scholar 

  • F. Rousset (2000) ArticleTitleGenetic differentiation between individuals J. Evol. Biol. 13 58–62 Occurrence Handle10.1046/j.1420-9101.2000.00137.x

    Article  Google Scholar 

  • C. Saenz-Romero R. P. Curies A. I. Monk (2001) ArticleTitleLandscape genetic structure of Pinus banksiana: allozyme variation Canad. J. Bot. 79 871–878 Occurrence Handle10.1139/cjb-79-8-871 Occurrence Handle1:CAS:528:DC%2BD3MXmvFKrsr4%3D

    Article  CAS  Google Scholar 

  • K. L. Shea G. R. Furnier (2002) ArticleTitleGenetic variation and population structure in central and isolated populations of balsam fir, Abies balsamea (Pinaceae) Amer. J. Bot. 89 783–791

    Google Scholar 

  • Z. Šidák (1967) ArticleTitleConfidence regions for the means of multivariate normal distributions J. Am. Stat. Assoc. 62 626–633 Occurrence Handle10.2307/2283989

    Article  Google Scholar 

  • R. R. Sokal N. L. Oden (1978) ArticleTitleSpatial autocorrelation in biology. 1 Methodology. Biol. J. Linn. Soc. 10 199–228

    Google Scholar 

  • D. E. Soltis C. H. Haufler D. C. Darrow G. J. Gastony (1983) ArticleTitleStarch gel electrophoresis of ferns: a compilation of grinding buffers, gel and electrode buffers, and staining schedules Amer. Fern J. 73 9–27 Occurrence Handle10.2307/1546611

    Article  Google Scholar 

  • B. R. Thomas S. E. Macdonald H. Hicks D. L. Adams R. B. Hodgetts (1999) ArticleTitleEffects on reforestation methods on genetic diversity of lodgepole pine: an assessment using microsatellite and randomly amplified polymorphic DNA markers Theor. Appl. Genet. 98 793–801 Occurrence Handle10.1007/s001220051136

    Article  Google Scholar 

  • F. Dyke ParticleVan (2003) Conservation biology: foundations, concepts, applications McGraw-Hill New York

    Google Scholar 

  • X. Vekemans O. J. Hardy (2004) ArticleTitleNew insights from fine-scale spatial genetic structure analysis in plant populations Molec. Ecol. 13 921–935 Occurrence Handle10.1046/j.1365-294X.2004.02076.x Occurrence Handle1:STN:280:DC%2BD2c7itlehug%3D%3D

    Article  CAS  Google Scholar 

  • G. G. Vendramin L. Lellle P. Rossi M. Morgante (1996) ArticleTitleA set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae Molec. Ecol. 5 595–598 Occurrence Handle10.1046/j.1365-294X.1996.00111.x Occurrence Handle1:CAS:528:DyaK28XlvFakt74%3D

    Article  CAS  Google Scholar 

  • D. B. Wagner (1992) ArticleTitleNuclear, chloroplast, and mitochondrial DNA polymorphisms as biochemical markers in population genetic analyses of forest trees New For. 6 373–390

    Google Scholar 

  • R. Walter B. K. Epperson (2004) ArticleTitleMicrosatellite analysis of spatial structure among seedlings in populations of Pinus strobus (Pinaceae) Amer. J. Bot. 91 549–557

    Google Scholar 

  • Wartenberg D. (1989) SAAP. A spatial autocorrelation analysis program version 4.3 Exeter Software, Setauket, New York.

  • B. S. Weir C. C. Cockerham (1984) ArticleTitleEstimating F-statistics for the analysis of population structure Evolution 38 1358–1370 Occurrence Handle10.2307/2408641

    Article  Google Scholar 

  • Wilson R. W., Jr., McQuilkin W. E. (1963) Silvical characteristics of eastern white pine. Research Paper NE-13. Upper Darby, PA: U.S. Department of Agriculture, Forest Service, Northeastern Forest Experiment Station. 29 p.

  • J. W. Wright (1953) ArticleTitlePollen-dispersion studies: some practical applications J. Heredity 31 114–118

    Google Scholar 

  • S. Wright (1922) ArticleTitleCoefficients of inbreeding and relationship Amer. Naturalist 56 330–338 Occurrence Handle10.1086/279872

    Article  Google Scholar 

  • S. Wright (1965) ArticleTitleThe interpretation of population structure by F-statistics with special regard to systems of mating Evolution 19 395–420 Occurrence Handle10.2307/2406450

    Article  Google Scholar 

  • Yeh F. C., Yang R. C., Boyle T. B. J. (1999) POPGENE version 1.31, Microsoft window-based free ware for population genetic analysis. Computer program and documentation distributed by University of Alberta and Centre for International Forestry Research, Alberta, Canada, website: http:/www.ualberta.ca/~fyeh/index.htm.

  • A. Young T. Boyle T. Brown (1996) ArticleTitleThe population genetics consequences of habitat fragmentation for plants Trends Ecol. Evol. 11 413–418 Occurrence Handle10.1016/0169-5347(96)10045-8

    Article  Google Scholar 

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Myers, E.R., Chung, M.Y. & Chung, M.G. Genetic diversity and spatial genetic structure of Pinus strobus (Pinaceae) across an island landscape inferred from allozyme and cpDNA markers. Plant Syst. Evol. 264, 15–30 (2007). https://doi.org/10.1007/s00606-006-0498-6

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