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Comparative phylogeography of two closely related Viola species occurring in contrasting habitats in the Japanese archipelago

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Abstract

Similar distribution ranges shared by closely related plant species may have been shaped through different migration histories if those species have differing habitat preference. To test this hypothesis, phylogeographical patterns and population genetic structures were compared between two sister Viola species: Viola eizanensis preferring woodland and V. chaerophylloides var. sieboldiana preferring grassland, both being native to the Japanese Archipelago. Amplified fragment length polymorphism (AFLP) was used for phylogenetic reconstruction, together with Bayesian ancestry analysis, AMOVA, analysis of genetic diversity statistics, and analysis of the relative contribution of each population to total diversity. The results indicated that V. eizanensis had two distinct lineages occurring in the western and eastern part of Japan, but such lineages are not distinct in V. chaerophylloides var. sieboldiana. Both species exhibited the low genetic diversity and high between-population differentiation typical of selfing plants. In V. chaerophylloides var. sieboldiana, one particular population made a significantly higher contribution to the total heterozygosity (H T), whereas in V. eizanensis, no population was identified as making a particularly higher contribution to H T. These findings suggest that V. eizanensis had been isolated in two large glacial refugia, whereas populations of V. chaerophylloides var. sieboldiana were restricted to a single small refuge. Different light requirements between these two closely related species probably caused these differing responses to climatic change during the last ice age.

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References

  • Arbogast BS, Kenagy GJ (2001) Comparative phylogeography as an integrative approach to historical biogeography. J Biogeogr 28:819–825

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Beardsley PM, Yen A, Olmstead RG (2003) AFLP phylogeny of Mimulus section Erythranthe and the evolution of hummingbird pollination. Evolution 57:1397–1410

    PubMed  CAS  Google Scholar 

  • Benvenuti S (2007) Weed seed movement and dispersal strategies in the agricultural environment. Weed Biol Manag 7:141–157

    Article  Google Scholar 

  • Bermingham E, Avise JC (1986) Molecular zoogeography of fresh-water fishes in the southeastern United States. Genetics 113:939–965

    PubMed  CAS  Google Scholar 

  • Bermingham E, Moritz C (1998) Comparative phylogeography: concepts and applications. Mol Ecol 7:367–369

    Article  Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    Article  PubMed  CAS  Google Scholar 

  • Bowen BW, Avise JC (1990) Genetic-structure of Atlantic and Gulf of Mexico populations of Sea Bass, Menhaden, and Sturgeon: influence of zoogeographic factors and life-history patterns. Mar Biol 107:371–381

    Article  Google Scholar 

  • Coart E, Vekemans X, Smulders MJM, Wagner I, Van Huylenbroeck J, Van Bockstaele E, Roldan-Ruiz I (2003) Genetic variation in the endangered wild apple (Malus sylvestris (L.) Mill.) in Belgium as revealed by amplified fragment length polymorphism and microsatellite markers. Mol Ecol 12:845–857

    Article  PubMed  CAS  Google Scholar 

  • Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86

    Article  Google Scholar 

  • Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626

    Article  PubMed  Google Scholar 

  • Cwynar LC, Macdonald GM (1987) Geographical variation of lodgepole pine in relation to population history. Am Nat 129:463–469

    Article  Google Scholar 

  • Dawson MN, Louie KD, Barlow M, Jacobs DK, Swift CC (2002) Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California transition zone. Mol Ecol 11:1065–1075

    Article  PubMed  CAS  Google Scholar 

  • Ditchfield AD (2000) The comparative phylogeography of neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals. Mol Ecol 9:1307–1318

    Article  PubMed  CAS  Google Scholar 

  • Dolan RW (1994) Patterns of isozyme variation in relation to population-size, isolation, and phytogeographic history in royal catchfly (Silene Regia Caryophyllaceae). Am J Bot 81:965–972

    Article  CAS  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial-DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  PubMed  CAS  Google Scholar 

  • Fujii N, Tomaru N, Okuyama K, Koike T, Mikami T, Ueda K (2002) Chloroplast DNA phylogeography of Fagus crenata (Fagaceae) in Japan. Plant Syst Evol 232:21–33

    Article  CAS  Google Scholar 

  • Fukuoka T, Matsui S (2002) Stratigraphy of pyroclastic deposits post-dating the AT tephra, Sanbe Volcano (in Japanese with English abstract). Earth Sci 56:105–122

    CAS  Google Scholar 

  • Gillespie JH (2004) Population genetics: a concise guide, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Gómez C, Espadaler X (1998) Myrmecochorous dispersal distances: a world survey. J Biogeogr 25:573–580

    Article  Google Scholar 

  • Hama E (2002) The wild violets of Japan in color. Seibundo-shinkasha, Tokyo

    Google Scholar 

  • Hare KM, Daugherty CH, Chapple DG (2008) Comparative phylogeography of three skink species (Oligosoma moco, O-smithi, O-suteri; Reptilia : Scincidae) in northeastern New Zealand. Mol Phylogenet Evol 46:303–315

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond Ser B Biol Sci 359:183–195

    Article  CAS  Google Scholar 

  • Hickerson MJ, Cunningham CW (2005) Contrasting quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution 59:344–360

    PubMed  Google Scholar 

  • Holsinger KE, Lewis PO, Dey DK (2002) A Bayesian approach to inferring population structure from dominant markers. Mol Ecol 11:1157–1164

    Article  PubMed  CAS  Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914

    Article  Google Scholar 

  • Igari M (1996) Violets of Japan (Nihon-no-sumire). Yama-to-keikoku-sha, Tokyo

    Google Scholar 

  • Jang SK, Lee WT, Yoo KO (2006) Taxonomic study on Viola albida var. albida and its related taxa (in Korean with English abstract). Korean J Plant Taxon 36:163–187

    Google Scholar 

  • Janssen P, Maquelin K, Coopman R, Tjernberg I, Bouvet P, Kersters K, Dijkshoorn L (1997) Discrimination of Acinetobacter genomic species by AFLP fingerprinting. Int J Syst Bacteriol 47:1179–1187

    Article  PubMed  CAS  Google Scholar 

  • Katoh S, Yamaguchi S, Inokuchi H, Okada A, Sakiyama T (2007) Late quaternary activity of the Kuresakatouge fault of the Yamasaki fault system in the Chugoku mountains, western Japan (in Japanese with English abstract). Human Nature 18:1–12

    Google Scholar 

  • Kawamoto Y, Shotake T, Nozawa K, Kawamoto S, Tomari K, Kawai S, Shirai K, Morimitsu Y, Takagi N, Akaza H, Fujii H, Hagihara K, Aizawa K, Akachi S, Oi T, Hayaishi S (2007) Postglacial population expansion of Japanese macaques (Macaca fuscata) inferred from mitochondrial DNA phylogeography. Primates 48:27–40

    Article  PubMed  Google Scholar 

  • Korpelainen H (2004) The evolutionary processes of mitochondrial and chloroplast genomes differ from those of nuclear genomes. Naturwissenschaften 91:505–518

    Article  PubMed  CAS  Google Scholar 

  • Kropf M, Kadereit JW, Comes HP (2003) Differential cycles of range contraction and expansion in European high mountain plants during the late quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 12:931–949

    Article  PubMed  CAS  Google Scholar 

  • Lönn M, Prentice HC, Tegelstrom H (1995) Genetic differentiation in hippocrepis-emerus (Leguminosae): allozyme and DNA fingerprint variation in disjunct Scandinavian populations. Mol Ecol 4:39–48

    Article  Google Scholar 

  • Maliouchenko O, Palmé AE, Buonamici A, Vendramin GG, Lascoux M (2007) Comparative phylogeography and population structure of European Betula species, with particular focus on B-pendula and B-pubescens. J Biogeogr 34:1601–1610

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–611

    Article  PubMed  CAS  Google Scholar 

  • Michaux JR, Libois R, Filippucci MG (2005) So close and so different: comparative phylogeography of two small mammal species, the Yellow-necked fieldmouse (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity 94:52–63

    Article  PubMed  CAS  Google Scholar 

  • Miyabuchi Y, Sugiyama S (2006) A 30,000-year phytolith record of tephra sequence, east of Aso caldera, southwestern Japan (in Japanese with English abstract). Q Res 45:15–28

    Article  Google Scholar 

  • Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends Ecol Evol 14:389–394

    Article  PubMed  Google Scholar 

  • Naruse T, Suzuki N, Inoue N, Toyoda S, Minowa T, Yasuba H, Yatagai S (2005) Depositional environmental changes over the past 30,000 years at Hosoike moor, Okayama prefecture, western Japan (in Japanese with English abstract). J Geogr 114:811–819

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical-Model for studying genetic-variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Newton AC, Allnutt TR, Gillies ACM, Lowe AJ, Ennos RA (1999) Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends Ecol Evol 14:140–145

    Article  PubMed  Google Scholar 

  • Ohi T, Kajita T, Murata J (2003) Distinct geographic structure as evidenced by chloroplast DNA haplotypes and ploidy level in Japanese Aucuba (Aucubacea). Am J Bot 90:1645–1652

    Article  Google Scholar 

  • Parendes LA, Jones JA (2000) Role of light availability and dispersal in exotic plant invasion along roads and streams in the H. J. Andrews Experimental Forest, Oregon. Conserv Biol 14:64–75

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  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 

  • Quérouil S, Verheyen E, Dillen M, Colyn M (2003) Patterns of diversification in two African forest shrews: Sylvisorex johnstoni and Sylvisorex ollula (Soricidae, Insectivora) in relation to paleo-environmental changes. Mol Phylogenet Evol 28:24–37

    Article  PubMed  Google Scholar 

  • R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Russell JR, Fuller JD, Macaulay M, Hatz BG, Jahoor A, Powell W, Waugh R (1997) Direct comparison of levels of genetic variation among barley accessions detected by RFLPs, AFLPs, SSRs and RAPDs. Theor Appl Genet 95:714–722

    Article  CAS  Google Scholar 

  • Sase T, Kato Y, Hosono M, Aoki K, Watanabe M (2006) The history of melanic horizons (“kurobokudo” horizons”) at the foot of Ashitaka Volcano, central Japan (in Japanese with English abstract). Earth Sci 60:147–163

    CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetic data analysis version 2.000. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Schönswetter P, Popp M, Brochmann C (2006) Rare arctic-alpine plants of the European Alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus. Mol Ecol 15:709–720

    Article  PubMed  CAS  Google Scholar 

  • Sharma SK, Knox MR, Ellis THN (1996) AFLP analysis of the diversity and phylogeny of Lens and its comparison with RAPD analysis. Theor Appl Genet 93:751–758

    Article  CAS  Google Scholar 

  • Soltis DE, Gitzendanner MA, Strenge DD, Soltis PS (1997) Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Syst Evol 206:353–373

    Article  Google Scholar 

  • Swofford DL (2000) PAUP*: phylogenetic analysis using parsimony (*and Other Methods). version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  PubMed  CAS  Google Scholar 

  • Takahara H, Sugita S, Harrison SP, Miyoshi N, Morita Y, Uchiyama T (2000) Pollen-based reconstructions of Japanese biomes at 0, 6000 and 18, 000 C-14 yr BP. J Biogeogr 27:665–683

    Article  Google Scholar 

  • Tiffney BH, Manchester SR (2001) The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere tertiary. Int J Plant Sci 162:S3–S17

    Article  Google Scholar 

  • Tsukada M (1985) Map of vegetation during the last glacial maximum in Japan. Q Res 23:369–381

    Article  Google Scholar 

  • Vekemans X (2002) AFLP-SURV. version 1.0. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium

    Google Scholar 

  • Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  PubMed  CAS  Google Scholar 

  • Yamada M, Hosoi E, Tamate H, Nagata J, Tatsuzawa S, Tado H, Ozawa S (2006) Distribution of two distinct lineages of sika deer (Cervus nippon) on Shikoku Island revealed by mitochondrial DNA analysis. Mammal Study 31:23–28

    Article  Google Scholar 

  • Yasuda SP, Minato S, Tsuchiya K, Suzuki H (2007) Onset of cryptic vicariance in the Japanese dormouse Glirulus japonicus (Mammalia, Rodentia) in the late tertiary, inferred from mitochondrial and nuclear DNA analysis. J Zool Syst Evol Res 45:155–162

    Article  Google Scholar 

  • Yoo KO, Jang SK, Lee WT (2005) Phylogeny of Korean Viola based on ITS sequences (in Korean with English abstract). Korean J Plant Taxon 35:7–23

    Google Scholar 

  • Zhang LB, Comes HP, Kadereit JW (2001) Phylogeny and quaternary history of the European montane/alpine endemic Soldanella (Primulaceae) based on ITS and AFLP variation. Am J Bot 88:2331–2345

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank all colleagues at the ecological laboratory of Kyushu University who provided helpful discussions, M. Igari, K. Miyoshi, K. Hosokawa, S. Masutani, M. Nagase, S. Tajiri and S. Baba for their help in locating study populations, M. Nakazawa and S. Tagane for technical instruction for AFLP experiments, and Chris Wood for correcting the English of the manuscript. Finally, this work was supported partially by a Grant-in-Aid for JSPS (Japan Society for the promotion of Science) Fellows to H.T.

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  1. Department of Biology, Faculty of Sciences, Kyushu University, 6-10-1, Hakozaki, Higashi-ku, Fukuoka, 812-8581, Japan

    Hironori Toyama & Tetsukazu Yahara

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  1. Hironori Toyama
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  2. Tetsukazu Yahara
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Correspondence to Hironori Toyama.

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Toyama, H., Yahara, T. Comparative phylogeography of two closely related Viola species occurring in contrasting habitats in the Japanese archipelago. J Plant Res 122, 389–401 (2009). https://doi.org/10.1007/s10265-009-0235-7

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