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Management units of the endangered herb Primula sieboldii based on microsatellite variation among and within populations throughout Japan

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Abstract

To promote programs for the conservation and restoration of the endangered species Primula sieboldii, we examined genetic variation at eight microsatellite loci among and within 32 remnant wild populations throughout Japan. Total allelic diversity within a population was higher in larger populations, but not so after rarefaction adjustment. The positive relationship between population size and the inbreeding coefficient may suggest that more heterozygous genets tend to survive the habitat contraction possibly because of the higher fitness associated with heterozygosity. By principal coordinate analysis and Bayesian analysis, we detected four genetic groups (Hokkaido, northern Honshu, central Honshu, and western Japan), which could be recognized as management units of P. sieboldii. If supplementation with plants from other populations were planned, it should be conducted among populations which belong to the same management unit and which are likely to represent the same adaptive variation.

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References

  • Bekessy SA, Ennos RA, Burgman MA, Newton AC, Ades PK (2003) Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biol Conserv 110:267–275

    Article  Google Scholar 

  • Cai HW, Wang XK, Morishima H (2004) Comparison of population genetic structures of common wild rice (Oryza rufipogon Griff.), as revealed by analyses of quantitative traits, allozymes, and RFLPs. Heredity 92:409–417

    Article  PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Demauro MM (1993) Relationship of breeding system to rarity in the lakeside daisy (Hymenoxys acaulis var. glabra). Conserv Biol 7:542–550

    Article  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  Google Scholar 

  • Environment Agency of Japan (2000) Threatened wildlife of Japan, red data book, vascular plants. Environment Agency of Japan, Tokyo (in Japanese)

    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 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    PubMed  CAS  Google Scholar 

  • Gompert Z, Nice CC, Fordyce JA, Forister ML, Shapiro AM (2006) Identifying units for conservation using molecular systematics: the cautionary tale of the Karner blue butterfly. Mol Ecol 15:1759–1768

    Article  PubMed  CAS  Google Scholar 

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

  • Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186

    Article  Google Scholar 

  • Hedrick P (2005) ‘Genetic restoration’: a more comprehensive perspective than ‘genetic rescue’. Trends Ecol Evol 20:109

    Article  PubMed  Google Scholar 

  • Hogbin PM, Peakall R (1999) Evaluation of the contribution of genetic research to the management of the endangered plant Zieria prostrata. Conserv Biol 13:514–522

    Article  Google Scholar 

  • Honjo M, Ueno S, Tsumura Y, Handa T, Washitani I, Ohsawa R (in press) Tracing the origins of stocks of the endangered species Primula sieboldii using nuclear microsatellites and chloroplast DNA. Conserv Genet

  • Honjo M, Ueno S, Tsumura Y, Washitani I, Ohsawa R (2004) Phylogeographic study based on intraspecific sequence variation of chloroplast DNA for the conservation of genetic diversity in the Japanese endangered species Primula sieboldii. Biol Conserv 120:215–224

    Article  Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Isagi Y, Honjo M, Washitani I (2001) Development of microsatellite markers for Primula sieboldii using degenerate oligonucleotide-primed PCR-amplified DNA. Mol Ecol Notes 1:22–24

    Article  CAS  Google Scholar 

  • Iwata H (2004) PCO ver. 1.0. Available from http://cse.naro.affrc.go.jp/iwatah/others/pco/index.html

  • Kery M, Matthies D, Spillman H (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88:17–30

    Article  Google Scholar 

  • Kitamoto N (2005) A reproductive biological study on the maintenance mechanism of genetic diversity of an endangered plant, Primula sieboldii. Doctoral dissertation, University of Tsukuba (in Japanese)

  • Kitamoto N, Honjo M, Ueno S, Takenaka A, Tsumura Y, Washitani I, Ohsawa R (2005a) Spatial genetic structure among and within populations of Primula sieboldii growing beside separate streams. Mol Ecol 14:149–157

    Article  CAS  Google Scholar 

  • Kitamoto N, Ueno S, Tsumura Y, Washitani I, Ohsawa R (2005b) Development of microsatellite markers in Primula sieboldii E. Morren, a threatened herb. Jpn J Conserv Ecol 10:47–51 (in Japanese with English summary)

    Google Scholar 

  • Luijten SH, Dierick A, Oostermeijer GB, Rajimann LEL, den Nijs HCM (2000) Population size, genetic variation, and reproductive success in a rapidly declining, self-incompatible perennial (Arnica montana) in the Netherlands. Conserv Biol 14:1776–1787

    Article  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Matsumura C, Washitani I (2000) Effects of population size and pollinator limitation on seed-set of Primula sieboldii populations in a fragmented landscape. Ecol Res 15:307–322

    Article  Google Scholar 

  • Mckay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Montalvo AM, Ellstrand NC (2001) Nonlocal transplantation and outbreeding depression in the subshrub Lotus scoparius (Fabaceae). Am J Bot 88:258–269

    Article  PubMed  Google Scholar 

  • Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Nagai M, Watanabe A, Nishihiro J, Washitani I (2006) The mating system and inbreeding depression. In: Washitani I (ed) Conservation molecular genetic ecology on Primula sieboldii. University of Tokyo Press, Tokyo, pp 240–258 (in Japanese)

    Google Scholar 

  • Nei M, Roychoudhury AK (1974) Sampling variance of heterozygosity and genetic distance. Genetics 76:379–390

    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, Wakabayashi M, Wu S, Murata J (2003) Phylogeography of Stachyurus praecox (Stachyuraceae) in the Japanese archipelago based on chloroplast DNA haplotypes. J Jpn Bot 78:1–14

    Google Scholar 

  • Ohshima K (1990) The history of straits around the Japanese islands in the late-Quaternary. Quat Res 29:193–208 (in Japanese with English summary)

    Article  Google Scholar 

  • Oostermeijer JGB, van Eijck MW, van Leeuwen NC, den Nijs JCM (1995) Analysis of the relationship between allozyme heterozygosity and fitness in the rare Gentiana pneumonanthe L. J Evol Biol 8:739–759

    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 

  • Pritchard JK, Wen W (2003) Documentation for Structure Software: Version 2. http://pritch.bsd.uchicago.edu

  • Rajimann LEL, van Leeuwen NC, Kersten R, Oostermeijer JGB, den Nijs HCM, Menken SBJ (1994) Genetic variation and outcrossing rate in relation to population size in Gentiana pneumonanthe L. Conserv Biol 8:1014–1026

    Article  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    PubMed  CAS  Google Scholar 

  • Robichaux RH, Friar EH, Mount DW (1997) Molecular genetic consequences of a population bottleneck associated with reintroduction of the Mauna Kea silversword (Argyroxiphium sandwicense ssp. sandwicense [Asteraceae]). Conserv Biol 11:1140–1146

    Article  Google Scholar 

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Schaal BA, Levin DA (1976) The demographic genetics of Liatris cylindracea Michx. (Compositae). Am Nat 110:191–206

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Soltis PS, Gitzendanner MA (1999) Molecular systematics and the conservation of rare species. Conserv Biol 13:471–483

    Article  Google Scholar 

  • Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135:367–374

    PubMed  CAS  Google Scholar 

  • Steinger T, Haldimann P, Leiss KA, Muller-Scharer H (2002) Does natural selection promote population divergence? A comparative analysis of population structure using amplified fragment length polymorphism markers and quantitative traits. Mol Ecol 11:2583–2590

    Article  PubMed  CAS  Google Scholar 

  • Tomaru N, Mitsutsuji T, Takahashi M, Tsumura Y, Uchida K, Ohba K (1997) Genetic diversity in Fagus crenata (Japanese beech): influence of the distributional shift during the late-Quaternary. Heredity 78:241–251

    Article  Google Scholar 

  • Tomaru N, Takahashi M, Tsumura Y, Takahashi M, Ohba K (1998) Intraspecific variation and phylogeographic patterns of Fagus crenata (Fagaceae) mitochondrial DNA. Am J Bot 85:629–636

    Article  CAS  Google Scholar 

  • Ueno S, Kitamoto N, Ohsawa R, Tsumura Y, Washitani I (2005) Nine additional microsatellite markers for Primula sieboldii E. Morren. Conserv Genet 6:1063–1064

    Article  Google Scholar 

  • Ueno S, Tsumura Y, Washitani I (2003) Development of microsatellite markers in Primula sieboldii E. Morren, a threatened Japanese perennial herb. Conserv Genet 4:809–811

    Article  CAS  Google Scholar 

  • Walter R, Epperson BK (2001) Geographic pattern of genetic variation in Pinus resinosa: area of greatest diversity is not the origin of postglacial populations. Mol Ecol 10:103–111

    Article  PubMed  CAS  Google Scholar 

  • Washitani I, Kabaya H (1988) Germination responses to temperature responsible for the seedling emergence seasonability of Primula sieboldii E. Morren in its natural habitat. Ecol Res 3:9–20

    Article  Google Scholar 

  • Washitani I, Kato M, Nishihiro J, Suzuki K (1995) Importance of queen bumble bees as pollinators facilitating inter-morph crossing in Primula sieboldii. Plant Sp Biol 9:169–176

    Article  Google Scholar 

  • Washitani I, Namai H, Osawa R, Niwa M (1991) Species biology of Primula sieboldii for the conservation of its lowland-habitat population: I. Inter-clonal variations in the flowering phenology, pollen load and female fertility components. Plant Sp Biol 6:27–37

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Yamazaki T (1993) Primula. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan 3a. Kodansha, Tokyo, pp 87–94

  • Yang RC (1998) Estimating hierarchical F-statistics. Evolution 52:950–956

    Article  Google Scholar 

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Acknowledgments

We express our sincere thanks to M. Ajima, S. Araki, M. Haga, H. Hata, M. Ide, Y. Kameyama, T. Kamijo, the Karuizawa Primrose Conservation Society, Y. Kato, K. Kida, T. Konishi, T. Kuwabara, K. Kuwata, M. Maeda, C. Matsumura, M. Mochida, H. Nakagaito, C. Nakano, M. Nakamura, J. Nishihiro, S. Ogawa, K. Oh, T. Ohmori, N. Ohtaki, T. Omozaki, A. Shinohara, K. Shirakawa, A. Suzuki, T. Suzuki, Y. Takahashi, Y. Takeda, T. Tsuchiya, S. Yamamoto, K. Yamanaka, J. Yokoyama, M. Yoshii, and Y. Yoshioka for collection of plant materials, and to anonymous reviewers for their comments for improving this paper. We also thank T. Kado and the members of the Laboratory of Plant Breeding at the University of Tsukuba for their assistance. This work was partly supported by the Fundamental Research Fund for Future Environment from the Japan Ministry of Environment.

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Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, 305-8572, Japan

    Masanori Honjo, Naoko Kitamoto & Ryo Ohsawa

  2. Department of Forest Genetics, Forestry and Forest Products Research Institute, Tsukuba, Ibaraki, 305-8687, Japan

    Saneyoshi Ueno & Yoshihiko Tsumura

  3. Graduate School of Agricultural and Life Science, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Masanori Honjo & Izumi Washitani

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  1. Masanori Honjo
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  2. Naoko Kitamoto
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  4. Yoshihiko Tsumura
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Correspondence to Masanori Honjo.

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Honjo, M., Kitamoto, N., Ueno, S. et al. Management units of the endangered herb Primula sieboldii based on microsatellite variation among and within populations throughout Japan. Conserv Genet 10, 257–267 (2009). https://doi.org/10.1007/s10592-007-9292-4

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