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Conflict in outcomes for conservation based on population genetic diversity and genetic divergence approaches: a case study in the Japanese relictual conifer Sciadopitys verticillata (Sciadopityaceae)

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Abstract

A major goal of conservation genetics is to determine which specific populations are most crucial for in situ or ex situ conservation. Genetic divergence and diversity are the two foundations by which priorities for conservation are typically determined. However, these measures may be confounded when past bottlenecks reduce genetic diversity of populations but also lead to their divergence. This study examines the potential conflicts in population prioritization for a relictual Japanese endemic conifer, Sciadopitys verticillata using nuclear microsatellites. High genetic structuring at the nuclear level compared to many other conifers (Fst = 0.129) was observed across the species range along with significant differences in genetic diversity between southern and northern populations. Conflict among genetic diversity and divergence population prioritization methods was observed in populations at the southwestern range edge of Kyushu and Chugoku, which were the most genetically distinct but also harboured the lowest diversity (Kyushu, He = 0.288, Ar = 2.172, and Chugoku, He = 0.222, Ar = 2.010). These populations contained only a subset of the genetic diversity found in Central Honshu and the Kii Peninsula (Central Honshu, He = 0.347, Ar = 2.707 and the Kii Peninsula, He = 0.337, Ar = 2.683), suggesting a reduction in genetic diversity as a result of bottlenecks. To determine if these highly bottlenecked populations in southwestern Japan are on the trajectory to extinction, or, conversely, if they harbour important genetic variation that has been fixed at the southwestern edge of the species range, common garden experiments are recommended in the future.

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References

  • Alvarez-Buylla ER, Garcia-Barrios R, Lara-Moreno C, Martinez-Ramos M (1996) Demographic and genetic models in conservation biology: applications and perspectives for tropical rain forest tree species. Annu Rev Ecol Syst 27:387–421

    Article  Google Scholar 

  • Antao T, Lopes A, Lopes R, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinform 9:323

    Article  Google Scholar 

  • Baalsrud HT (2011) Population characteristics and estimates of effective population size in a house sparrow metapopulation. Norwegian University of Science and Technology, Trondheim

  • Beaumont MA, Nichols RA (1996) Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond Ser B-Biol Sci 263:1619–1626

    Article  Google Scholar 

  • Benkman CW (1995) Wind dispersal capacity of pine seeds and the evolution of different seed dispersal modes in pines. Oikos 73:221–224

    Article  Google Scholar 

  • Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627

    PubMed  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  CAS  PubMed  Google Scholar 

  • Caballero A, Rodriguez-Ramilo ST (2010) A new method for the partition of allelic diversity within and between subpopulations. Conserv Genet 11:2219–2229

    Article  Google Scholar 

  • Cavers S, Navarro C, Lowe AJ (2004) Targeting genetic resource conservation in widespread species: a case study of Cedrela odorata L. For Ecol Manage 197:285–294

    Article  Google Scholar 

  • Cavers S, Degen B, Caron H, Lemes M, Margis R, Salgueiro F, Lowe A (2005) Optimal sampling strategy for estimation of spatial genetic structure in tree populations. Heredity 95:281–289

    Article  CAS  PubMed  Google Scholar 

  • Cornuet J, Luikart G (1996) Description and power analysis of two tests for detecting recent bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crisp MD, Cook LG (2011) Cenozoic extinctions account for the low diversity of extant gymnosperms compared with angiosperms. The New phytologist 192:997–1009

    Article  CAS  PubMed  Google Scholar 

  • Dick CW, Abdul-Salim K, Bermingham E (2003) Molecular systematic analysis reveals cryptic tertiary diversification of a widespread tropical rain forest tree. Am Nat 162:691–703

    Article  PubMed  Google Scholar 

  • Earl DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Eckenwalder JE (2009) Conifers of the world: the complete reference. Timber Press, New York

    Google Scholar 

  • Eckert C, Samis K, Lougheed S (2008) Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Ellis J, Burke J (2007) EST-SSRs as a resource for population genetic analyses. Heredity 99:125–132

    Article  CAS  PubMed  Google Scholar 

  • Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant species. Am J Bot 71(1):123–131

    Article  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  CAS  PubMed  Google Scholar 

  • Excoffier L, Hofer T, Foll M (2009) Detecting loci under selection in a hierarchically structured population. Heredity 103:285–298

    Article  CAS  PubMed  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Gitzendanner MA, Weekley CW, Germain-Aubrey CC, Soltis DE, Soltis PS (2012) Microsatellite evidence for high clonality and limited genetic diversity in Ziziphus celata (Rhamnaceae), an endangered, self-incompatible shrub endemic to the Lake Wales Ridge, Florida, USA. Conserv Genet 13:223–234

    Article  CAS  Google Scholar 

  • Gómez A, Carvalho GR (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Mol Ecol 9:203–214

    Article  PubMed  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Halkett F, Simon J-C, Balloux F (2005) Tackling the population genetics of clonal and partially clonal organisms. Trends Ecol Evol 20:194–201

    Article  PubMed  Google Scholar 

  • Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. Population genetics of forest trees. Springer, Berlin, pp 95–124

    Chapter  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Hiraoka K, Tomaru N (2009a) Genetic divergence in nuclear genomes between populations of Fagus crenata along the Japan Sea and Pacific sides of Japan. J Plant Res 122:269–282

    Article  CAS  PubMed  Google Scholar 

  • Hiraoka K, Tomaru N (2009b) Population genetic structure of Fagus japonica revealed by nuclear microsatellite markers. Int J Plant Sci 170:748–758

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jeffreys H (1961) Theory of probability. Oxford University Press, Oxford, UK

  • Jones RC, Steane DA, Lavery M, Vaillancourt RE, Potts BM (2012) Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex. Ecol Evol 3:1–17

    Article  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Katsuki T, Luscombe D, Farjon A (2013) Sciadopitys verticillata. In: IUCN 2013 IUCN Red list of threatened species, www.iucnredlist.org. Accessed 23 Aug 2013

  • Kawase D, Ueno S, Tsumura Y, Tomaru N, Seo A, Yumoto T (2009) Development and characterization of EST-SSR markers for Sciadopitys verticillata (Sciadopityaceae). Conserv Genet 10:1997–1999

    Article  Google Scholar 

  • Kawase D, Tsumura Y, Tomaru N, Seo A, Yumoto T (2010) Genetic structure of an endemic Japanese conifer, Sciadopitys verticillata (Sciadopityaceae), by using microsatellite markers. J Hered 101:292

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Allendorf F, Cornuet J, Sherwin W (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto A, Uchida K, Taguchi Y, Tani N, Tsumura Y (2010) Genetic diversity and structure of natural fragmented Chamaecyparis obtusa populations as revealed by microsatellite markers. J Plant Res 123:689–699

    Article  PubMed  Google Scholar 

  • Matthews JV, Ovenden LE (1990) Late tertiary plant macrofossils from localities in Arctic/Subarctic North America: a review of the data. Arctic 43:364–392

    Google Scholar 

  • McLachlan JS, Hellmann JJ, Schwartz MW (2007) A framework for debate of assisted migration in an era of climate change. Conserv Biol 21:297–302

    Article  PubMed  Google Scholar 

  • McPherson H, van der Merwe M, Delaney SK, Edwards MA, Henry RJ, McIntosh E, Rymer PD, Milner ML, Siow J, Rossetto M (2013) Capturing chloroplast variation for molecular ecology studies: a simple next generation sequencing approach applied to a rainforest tree. BMC Ecol 13:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Milligan B (1992) Plant DNA isolation. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. IRL Press, Oxford, pp 59–88

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, DellaSala D, Alaback P (2011) Temperate rainforests of Japan. In: DellaSala D (ed) Temperate and boreal rainforests of the world: ecology and conservation. Island Press, Washington

    Google Scholar 

  • Narum SR, Hess JE (2011) Comparison of FST outlier tests for SNP loci under selection. Mol Ecol Res 11:184–194

    Article  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular-data 2 Gene-frequency data. J Mol Evol 19:153–170

    Article  CAS  PubMed  Google Scholar 

  • Pariset L, Joost S, Marsan PA, Valentini A, Ecogene Consortium EC (2009) Landscape genomics and biased FST approaches reveal single nucleotide polymorphisms under selection in goat breeds of North-East Mediterranean. BMC Genet 10:1–8

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pérez-Figueroa A, Saura M, Fernández J, Toro M, Caballero A (2009) METAPOP—a software for the management and analysis of subdivided populations in conservation programs. Conserv Genet 10:1097–1099

    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 

  • Piry S, Luikart G, Cornuet J (1999) Computer note. Bottleneck: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scotti I, Paglia G, Magni F, Morgante M (2006) Population genetics of Norway spruce (Picea abies Karst.) at regional scale: sensitivity of different microsatellite motif classes in detecting differentiation. Ann For Sci 63:485–491

    Article  CAS  Google Scholar 

  • Sgro CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337

    Article  PubMed Central  Google Scholar 

  • Simaji K, Ito T (1988) Nihon no iseki shutudo mokuseihin souran. Yuzankaku Inc, Osaka, p 296

    Google Scholar 

  • Soto-Cerda BJ, Cloutier S (2013) Outlier loci and selection signatures of simple sequence repeats (SSRs) in flax (Linum usitatissimum L.). Plant Mol Biol Rep 31(4):978–990

  • Suzuki M (2002) Nihonjin to ki no bunka. Yasaka Shobou, Tokyo, p 253

    Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi T, Tani N, Taira H, Tsumura Y (2005) Microsatellite markers reveal high allelic variation in natural populations of Cryptomeria japonica near refugial areas of the last glacial period. J Plant Res 118:83–90

    Article  CAS  PubMed  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) COMPUTER PROGRAMS: onesamp: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Res 8:299–301

    Article  Google Scholar 

  • Tsumura Y (2006) The phylogeographic structure of Japanese coniferous species as revealed by genetic markers. Taxon 55:53–66

    Article  Google Scholar 

  • Uemura K (1986) A note on Tertiary Sciadopitys (Coniferopsida) from Japan. Bull Nat Sci Mus Tokyo Ser C 12:53–60

    Google Scholar 

  • Väli Ü, Einarsson A, Waits L, Ellegren H (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17:3808–3817

    Article  PubMed  Google Scholar 

  • van der Hammen T, Wijmstra TA, Zagwijn WH (1971) The floral record of the late cenozoic of Europe. In: Turekian KK (ed) Late cenozoic glacial ages. Yale University Press, New Haven

    Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Vilas A, Pérez-Figueroa A, Caballero A (2012) A simulation study on the performance of differentiation-based methods to detect selected loci using linked neutral markers. J Evol Biol 25:1364–1376

    Article  CAS  PubMed  Google Scholar 

  • Waples RS (2002) Definition and estimation of effective population size in the conservation of endangered species. In: Beissenger SR, McCullough DR (eds) Population viability analysis. University of Chicago Press, Chicago, pp 147–168

    Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756

    Article  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed Central  Google Scholar 

  • Wolfe AP, Tappert R, Muehlenbachs K, Boudreau M, McKellar RC, Basinger JF, Garrett A (2009) A new proposal concerning the botanical origin of Baltic amber. Proc R Soc B: Biol Sci 276:3403–3412

    Article  CAS  Google Scholar 

  • Worth JRP, Sakaguchi S, Tanaka N, Yamasaki M, Isagi Y (2013) Northern richness and southern poverty: contrasting genetic footprints of glacial refugia in the relictual tree Sciadopitys verticillata (Coniferales: Sciadopityaceae). Biol J Linn Soc 108:263–277

    Article  Google Scholar 

  • Yamada M (1993) Compilation of literature on archaeological wooden remains in Japan: history of human-plant relationship from the point of timber economy and species selection. Jpn J Hist Bot, Special Issue 1 (in Japanese)

  • Yamamoto S-I (1988) Seedling recruitment of Chamaecyparis obtusa and Sciadopitys verticillata in different microenvironments in an old-growth Sciadopitys verticillata forest. J Plant Res 101:61–71

    Google Scholar 

  • Young AG, Boshier D (2000) Forest conservation genetics: principles and practice. Csiro Publishing, Wallingford

    Google Scholar 

  • Yumoto T (2011) Historical perspectives on the relationships between humanity and nature in Japan. Landscape ecology in Asian cultures. Springer, New York, pp 3–10

    Chapter  Google Scholar 

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Acknowledgments

The authors thank H. Ando, S. Harasawa, Y. Hatanaka, D. Kawase, T. Mizuno, L. Mizusawa, T. Oda, S. Sakaguchi, M. Suzuki, and Y. Yamazaki for assistance in the field, and K. Ohba for valuable advice on this study. We also thank Mizuno Tadakuni of the Wakayama prefecture government and Nakamori Yumiko of the Wakayama Prefecture Museum for help with sampling in Wakayama Prefecture. Lastly we also thank the Field Science Centre for Northern Biosphere, Hokkaido University, Kyushu University Forest- Seto Regional Forest Office, Kiso Regional Forest Office, Mima City Government Office and the Omogo Mountain Museum for sampling assistance and permission. This research was supported by a Japanese Society for the Promotion of Science research fellowship awarded to JRPW and by the program of the Global Environmental Research of Japan (S-8), the Ministry of the Environment.

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Worth, J.R.P., Yokogawa, M., Pérez-Figueroa, A. et al. Conflict in outcomes for conservation based on population genetic diversity and genetic divergence approaches: a case study in the Japanese relictual conifer Sciadopitys verticillata (Sciadopityaceae). Conserv Genet 15, 1243–1257 (2014). https://doi.org/10.1007/s10592-014-0615-y

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