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Chloroplast DNA assessment of anagenetic speciation in Rubus takesimensis (Rosaceae) on Ulleung Island, Korea

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Abstract

Two major modes of speciation, i.e., cladogenesis and anagenesis, have often been used to explain the generation of distinct plant diversity on oceanic islands. Anagenetic speciation is of particular interest to plant endemics on Ulleung Island, Korea because, of nearly 40 endemics, approximately 88% or even all endemic species are thought to be anagenetically derived. Despite its important role in Ulleung Island, the full scope of the anagenetic speciation and the genetic consequences of this speciation mode have been limited to a very few families (i.e., Apiaceae, Sapindaceae, and Ranunculaceae). Based on extensive sampling (a total of 322 individuals) and trnL-F cpDNA noncoding sequences, we conducted phylogenetic and haplotype network analyses for the species pair of Rubus crataegifolius (continental progenitor)-R. takesimensis (insular derivative). Rubus takesimensis on Ulleung Island is not a monophyletic group, suggesting at least two independent introductions from geographically and genetically divergent source populations. No significant reduction in cpDNA haplotype diversity and genetic differentiation in R. takesimensis are consistent with expectations from the anagenetically derived species. A further study based on comprehensive sampling and more variable molecular markers will shed light into the genetic consequences of anagenetic speciation in Rubus on Ulleung Island.

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References

  • Alice LA, Campbell CS (1999) Phylogeny of Rubus (Rosaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Am J Bot 86:81–97

    Article  CAS  PubMed  Google Scholar 

  • Baldwin BG, Kyhos DW, Dvorak J, Carr GD (1991) Chloroplast DNA evidence for a North American origin of the Hawaiian silversword alliance (Asteraceae). Proc Natl Acad Sci USA 88:1840–1843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Böehl UR, Hilger HH, Martin WF (1996) Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proc Natl Acad Sci USA 93:11740–11745

    Article  Google Scholar 

  • Carlquist S (1974) Island biology. New York: Columbia University Press

    Book  Google Scholar 

  • Carr GD (1985) Monography of the Hawaiian Madiinae (Asteraceae): Argyroxiphium, Dabautia, and Wilkesia. Allertonia 4:1–123

    Google Scholar 

  • Caujapé-Castells J, Tye A, Crawford DJ, Santos-Guerra A, Sakai A, Beaver K, Lobin W, Vincent Florens FB, Moura M, Jardim R, Gómes I, Kueffer C (2010) Conservation of oceanic island floras: present and future global challenges. Perspect Plant Ecol Evol Syst 21:107–129

    Article  Google Scholar 

  • Chae SH, So S, Han K, Kim M, Park SH, Lee J (2007) A taxonomic review of Phytolacca insularis (Phytolaccaceae). Korean J Pl Taxon 37:431–446

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Crawford DJ, Stuessy TF (2016) Cryptic variation, molecular data, and the challenge of conserving plant diversity in oceanic archipelagos: the critical role of plant systematics. Korean J Pl Taxon 46:129–148

    Article  Google Scholar 

  • Crawford DJ, Stuessy TF, Cosner MB, Haines DW, Silva OM, Baeza M (1992) Evolution of the genus Dendroseris (Asteraceae: Lactuceae) on the Juan Fernandez Islands: evidence from chloroplast and ribosomal DNA. Syst Bot 17:676–682

    Article  Google Scholar 

  • Darwin C (1842) The structure and distribution of coral reefs. London: Smith, Elder and Co

    Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection (reprint of first edition, 1950). Watts & Co., London

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11015

    Google Scholar 

  • Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966

    Article  CAS  PubMed  Google Scholar 

  • Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant population. Heredity 72:250–259

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Focke WO (1910) Species Ruborum monographiae generis Rubi prodromus. Bibl Bot 17:1–120

    Google Scholar 

  • Focke WO (1911) Species Ruborum monographiae generis Rubi prodromus. Bibl Bot 17:121–223

    Google Scholar 

  • Focke WO (1914) Species Ruborum monographiae generic Rubi prodromus. Bibl Bot 19:224–498

    Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  • Givnish TJ, Sytsma KJ, Smith JF, Hahn WJ (1994) Thorn-like prickles and heterophylly in Cyanea: adaptations to extinct avian browsers on Hawaii? Proc Natl Acad Sci USA 91:2810–2814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gustafsson A (1942) The origin and properties of the European blackberry flora. Hereditas 28:249–277

    Article  Google Scholar 

  • Gustafsson A (1943) The genesis of the European blackberry flora. Lunds Universitets Årsskrift 39:1–200

    Google Scholar 

  • Hart MW, Sunday J (2007) Things fall apart: Biological species form unconnected parsimony networks. Biol Lett 3:509–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howarth DG, Gardner DE, Morden CW (1997) Phylogeny of Rubus subgenus Idaeobatus (Rosaceae) and its implications toward colonization of the Hawaiian Islands. Syst Bot 22:433–441

    Article  Google Scholar 

  • Hummer KE (1996) Rubus diversity. HortScience 31:182–183

    Google Scholar 

  • Jeong KS, Kim MS, Lee W, Pak JH (2014) Intraspecific variation and geographic study of Lonicera insularis (Caprifoliaceae) based on chloroplast DNA sequences. Korean J Pl Taxon 44:202–207

    Article  Google Scholar 

  • Kim YK (1985) Petrology of Ulreung volcanic island, Korea–part 1. Geology. J Japanese Assoc Mineral Petrol Econ Geol 80:128–135

    Article  Google Scholar 

  • Kim JW (1988) The phytosociology of forest vegetation on Ulreungdo, Korea. Phytocoenologia 16:128–135

    Google Scholar 

  • Kim SC, Crawford DJ, Francisco-Ortega J, Santos-Guerra A (1996) A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proc Natl Acad Sci USA 93:7743–7748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreft H, Jetz W, Mutke J, Kier G, Barthlott W (2008) Global diversity of island floras from a macroecological perspective. Ecol Lett 11:116–127

    PubMed  Google Scholar 

  • Lee JH, Lee DH, Choi BH (2013) Phylogeography and genetic diversity of East Asian Neolitsea sericea (Lauraceae) based on variations in chloroplast DNA sequences. J Plant Res 126:193–202

    Article  PubMed  Google Scholar 

  • Lee W, Pak JH (2010) Intraspecific sequence variation of trnL/F intergenic region (cpDNA) in Sedum takesimense Nakai (Crassulaceae) and aspects of geographic distribution. Korean J Pl Taxon 40:157–162

    Google Scholar 

  • Levy F, Neal CL (1999) Spatial and temporal genetic structure in chloroplast and allozyme markers in Phacelia dubia implicate genetic drift. Heredity 82:422–431

    Article  CAS  PubMed  Google Scholar 

  • Li EX, Yi S, Qiu YX, Guo JT, Comes HP, Fu CX (2008) Phylogeography of two East Asian species in Croomia (Stemonaceae) inferred from chloroplast DNA and ISSR fingerprinting variation. Mol Phylogenet Evol 49:702–714

    Article  CAS  PubMed  Google Scholar 

  • Lu LT (1983) A study on the genus Rubus of China. Acta Phytotaxon Sin 21:13–25

    Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biologeography. Princeton University Press, Princeton

    Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade version 3.04 Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • McCauley DE, Stevens JE, Peroni PA, Ravelli JA (1996) The spatial distribution of chloroplast DNA and allozyme polymorphisms within a population of Silene alba (Caryophyllaceae). Am J Bot 83:727–731

    Article  CAS  Google Scholar 

  • Muller K (2005) SeqState–primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinformatics 4:65–69

    Article  PubMed  Google Scholar 

  • Nakai T (1918) Notulae ad plants Japoniae et Koreae XVII. Bot Mag Tokyo 32:104–105

    Google Scholar 

  • Oh SH (2015) Sea, wind, or bird: origin of Fagus multinervis (Fagaceae) inferred from chloroplast DNA sequences. Korean J Pl Taxon 45:213–220

    Article  Google Scholar 

  • Oh SH, Chen L, Kim SH, Kim YD, Shin HC (2010) Phylogenetic relationship of Physocarpus insularis (Rosaceae) endemic on Ullung Island: Implications for Conservation Biology. J Plant Biol 53:94–105

    Article  Google Scholar 

  • Pfosser M, Guzy-Wróbelska J, Sun BY, Stuessy TF, Sugawara T, Fujii N (2002) The origin of species of Acer (Sapindaceae) endemic to Ullung Island, Korea. Syst Bot 27:351–367

    Google Scholar 

  • Pfosser M, Jakubowsky G, Schlüter PM, Fer T, Kato H, Stuessy TF, Sun BY (2006) Evolution of Dystaenia takesimana (Apiaceae), endemic to Ullung Island, Korea. Plant Syst Evol 256:159–170

    Article  Google Scholar 

  • Pfosser M, Sun BY, Stuessy TF, Jang CG, Guo YP, Kim TJ, Hwan KC, Kato H, Sugawara T (2011) Phylogeny of Hepatica (Ranunculaceae) and origin of Hepatica maxima Nakai endemic to Ullung Island, Korea. Stapfia 95:16–27

    Google Scholar 

  • Qi XS, Chen C, Comes HP, Sakaguchi S, Liu YH, Tanaka N, Sakio H, Qiu YX (2012) Molecular data and ecological nich emodelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphylluum (Cercidiphyllaceae). New Phytol 196:617–630

    Article  CAS  PubMed  Google Scholar 

  • Qi XS, Yuan N, Comes HP, Sakaguchi S, Qiu YX (2014) A strong ‘filter’ effect of the East China Sea land bridge for East Asia’s temperate plant species: inferences from molecular phylogeography and ecological niche modeling of Platycrater arguta (Hydrangeaceae). BMC Evol Biol 14:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu YX, Qi XS, Jin XF, Tao XY, Fu CX, Naiki A, Comes HP (2009a) Population genetic structure, phylogeography, and demographic history of Platycrater arguta (Hydrangeaceae) endemic to East China and South Japan, inferred from chloroplast DNA sequence variation. Taxon 58:1226–1241

    Google Scholar 

  • Qiu YX, Sun Y, Zhang XP, Lee J, Fu CX, Comes HP (2009b) Molecular phylogeography of East Asian Kirengeshoma (Hydrangeaceae) in relation to Quaternary climate change and landbridge configurations. New Phytol 183:480–495

    Article  CAS  PubMed  Google Scholar 

  • Robertson KR (1974) The genera of Rosaceae in southeastern United States. J Arnold Arboretum 55:352–360

    Google Scholar 

  • Sakaguchi S, Qiu YX, Liu YH, Qi XS, Kim SH, Han J, Takeuchi Y, Worth JR, Yamasaki M, Sakurai S (2012) Climate oscillation during the Quaternary associated with landscape heterogeneity prompted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Mol Ecol 21:3823–3838

    Article  PubMed  Google Scholar 

  • Sang T, Crawford DJ, Kim SC, Stuessy TF (1994) Radiation of the endemic genus Dendroseris (Asteraceae) on the Juan Fernandez Islands: evidence from sequences of the ITS region of nuclear ribosomal DNA. Am J Bot 81:1494–1501

    Article  CAS  Google Scholar 

  • Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: The tortoise and the hare III. Am J Bot 94:275–288

    Article  CAS  PubMed  Google Scholar 

  • Simmon MP, Ochoterena H (2000) Gaps as characters in sequencebased phylogenetic analyses. Syst Biol 49:369–381

    Article  Google Scholar 

  • Stuessy TF (2007) Evolution of specific and genetic diversity during ontogeny of island floras: the importance of understanding process for interpreting island biogeographic patterns. In: Ebach MC, Tangney RS (eds). Biogeography in a changing world. CRC Press, Boca Raton, pp 117–133

    Google Scholar 

  • Stuessy TF, Jakubowsky G, Gómez RS, Pfosser M, Schlüter PM, Fer T, Sun BY, Kato H (2006) Anagenetic evolution in island plants. J Biogeo 33:1259–1265

    Article  Google Scholar 

  • Stuessy TF, Takayama K, López-Sepúlveda P, Crawford DJ (2014) Interpretation of patterns of genetic variation in endemic plant species of oceanic islands. Bot J Linn Soc 174:276–288

    Article  PubMed  Google Scholar 

  • Sun BY, Stuessy TF (1998) Preliminary observations on the evolution of endemic angiosperms of Ullung Island, Korea. In: Stuessy TF, Ono M (eds) Evolution and speciation of island plants. Cambridge University Press, New York, pp 181–202

    Chapter  Google Scholar 

  • Sun BY, Shin H, Hyun JO, Kim YD, Oh SH (2014) Vascular plants of Dokdo and Ulleungdo Islands in Korea. The National Institute of Biological Resources, GeoBook Publishing Co, Korea

    Google Scholar 

  • Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (and other method). Version 4.0b10. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  CAS  PubMed  Google Scholar 

  • Takayama K, Sun BY, Stuessy TF (2012) Genetic consequences of anagenetic speciation in Acer okamotoanum (Sapindaceae) on Ullung Island, Korea. Ann Bot 109:321–330

    Article  PubMed  Google Scholar 

  • Takayama K, Sun BY, Stuessy TF (2013) Anagenetic speciation in Ullung Island, Korea: genetic diversity and structure in the island endemic species, Acer takesimense (Sapindaceae). J Plant Res 126:323–333

    Article  PubMed  Google Scholar 

  • Takayama K, López-Sepúlveda P, Greimler J, Crawford DJ, Peñailillo P, Baeza M, Ruiz E, Kohl G, Tremetsberger K, Gatica A, Letelier L, Novoa P, Novak J, Stuessy TF (2015) Genetic consequences of cladogenetic vs. anagenetic speciation in endemic plants on oceanic islands. AoB Plants 7: plv102, Doi:10.1093/aobpla/pvl102

    Article  PubMed  PubMed Central  Google Scholar 

  • Thompson MM (1995) Chromosome numbers of Rubus species at the National Clonal Germplasm Repository. HortScience 30: 1447–1452

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higins DG (1997) The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace AR (1881) Island life. London: Macmillan and Co

    Google Scholar 

  • Wang JF, Gong X, Chiang YC, Kuroda C (2013) Phylogenetic patterns and disjunct distribution in Ligularia hodgsonii Hook. (Asteraceae). J Biogeogr 40:1741–1754

    Article  Google Scholar 

  • Waugh R, Van Den Ven WTG, Phillips MS, Powell W (1990) Chloroplast DNA diversity in the genus Rubus (Rosaceae) revealed by Southern hybridization. Pl Syst Evol 172:65–75

    Article  CAS  Google Scholar 

  • Weber HE (1996) Former and modern taxonomic treatment of the apomictic Rubus complex. Folia Geobot Phytotaxon 31:373–380.

    Article  Google Scholar 

  • Whittaker RJ (1998) Island biogeography. Oxford University Press, Oxford

    Google Scholar 

  • Yang JY, Yoon HS, Pak JH (2012) Phylogeny of Korean Rubus (Rosaceae) based on the second intron of the LEAFY gene. Can J Plant Sci 92:461–472

    Article  CAS  Google Scholar 

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Correspondence to Jae-Hong Pak or Seung-Chul Kim.

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Lee, W., Yang, J., Jung, KS. et al. Chloroplast DNA assessment of anagenetic speciation in Rubus takesimensis (Rosaceae) on Ulleung Island, Korea. J. Plant Biol. 60, 163–174 (2017). https://doi.org/10.1007/s12374-016-0421-9

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