Skip to main content
SpringerLink
Log in

Insights from Chloroplast DNA into the Progenitor-Derivative Relationship Between Campanula punctata and C. takesimana (Campanulaceae) in Korea

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Of the nearly 40 endemics present on Ulleung Island, Campanula takesimana Nakai represents an anagenetically derived lineage of a continental progenitor, C. punctata Lam. Other than its low morphological divergence, little is known about the genetic diversity and population structure of the species pair or the geographical origin of C. takesimana. We sampled a total of 240 accessions in 22 populations, including one Dokdo Island population, of the two species, sequenced four noncoding chloroplast regions (rps16-trnK, trnQ-rps16, psbD-trnT, and psbM-trnD; 4482 bp), and assessed the genetic consequences of anagenetic speciation. Based on chloroplast DNA, we found substantially lower genetic diversity statistics for C. takesimana compared to its progenitor, significant population genetic structuring in insular derivative species, and significant molecular divergence between C. punctata and C. takesimana. Mutually exclusive haplotypes were found in the two species, and the haplotype network suggested that Ulleung Island haplotypes were derived from the Dokdo Island haplotype, which was originally derived from a C. punctata population in Bonghwa-gun, Gyeongsangbuk-do Province. This study pinpoints a very narrow geographical source area and suggests the potentially important role of Dokdo Island as an initial stepping stone for Ulleung Island endemics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Birky CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    CAS  PubMed  Google Scholar 

  • Emerson BC, Patiño J (2018) Anagenesis, cladogenesis, and speciation on islands. Trends Ecol Evol 33:488–491

    PubMed  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

    PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gil H-Y, Maki M, Pimenova EA, Taran A, Kim S-C (2020) Origin of the critically endangered endemic species Scrophularia takesimensis (Scrophulariaceae) on Ulleung Island, Korea: implications for conservation. J Plant Res. https://doi.org/10.1007/s10265-020-01221-z

    Article  PubMed  Google Scholar 

  • Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16:700–706

    Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Havill N, Campbell CS, Vining T, LePage B, Bayer R, Donoghue M (2008) Phylogeny and biogeography of Tsuga (Pinaceae) inferred from nuclear ribosomal ITS and chloroplast DNA sequence data. Syst Bot 33:478–489

    Google Scholar 

  • Holman G, Del Tredici P, Havill N, Lee NS, Cronn R, Cushman K, Mathews S, Raubeson L, Campbell CS (2017) A new species and introgression in eastern Asian Hemlocks (Pinaceae: Tsuga). Syst Bot 42:733–746

    Google Scholar 

  • Hyun JO, Kwon SK (2006) Flora of Dokdo, report on the detailed survey of Dokdo ecosystem. Ministry of Environment, Seoul, pp 35–44

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Kim K-A, Yoo K-O (2012) Phylogenetic relationships of Korean Campanulaceae based on chloroplast DNA sequences. Korean J Pl Taxon 42:282–293

    Google Scholar 

  • Kim HJ, Shin BC, Jeung MY (2009) Research trend of Dokdo island plants-at focus of research data from 1947 to 2009. J Korean Inst Tradit Landsc Archit 27:61–78

    Google Scholar 

  • Kim K-A, Yoo K-O, Cheon K-S (2020) The complete chloroplast genome sequence of Campanula zangezura (Campanulaceae). Mitochondrial DNA B Resour 5:480–481

    PubMed  PubMed Central  Google Scholar 

  • Lee W, Pak J-H (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 

  • Lee S, Lee J, Kim S (1997) A new species of Adenophora (Campanulaceae) from Korea. J Plant Res 110:77–80

    CAS  PubMed  Google Scholar 

  • Lee W, Yang JY, Jung K-S, Pak J-H, Maki M, Kim S-C (2017) Chloroplast DNA assessment of anagenetic speciation in Rubus takesimensis (Rosaceae) on Ulleung Island, Korea. J Plant Biol 60:163–174

    CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Maddison WP, Maddison DR (2005) MacClade version 4.08 Analysis of phylogeny and character evolution. Sinauer Associates, Sunderland

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Palumbi SR, Cipriano F, Hare MP (2001) Predicting nuclear gene coalescence from mitochondrial data: the three-times rule. Evolution 55:859–868

    CAS  PubMed  Google Scholar 

  • Park K-R, Jung H-J (2000) Isozyme and morphological variation in Campanula punctata and C. takesimina (Campanulaceae). Korean J Pl Taxon 30:1–16

    Google Scholar 

  • Park C-W, Bhandari GS, Won H, Park JH, Park DS (2018) Polyploidy and introgression in invasive giant knotweed (Fallopia sachalinensis) during the colonization of remote volcanic islands. Sci Rep 8:16021

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Pfosser MF, Jakubowsky G, Schluter PM, Fer T, Kato H, Stuessy TF, Sun BY (2005) Evolution of Dystaenia takesimana (Apiaceae), endemic to Ulleung Island, Korea. Plant Syst Evol 256:159–170

    Google Scholar 

  • Rogers AR, Hapending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Roquet C, Sanmartín I, Garcia-Jacas N, Sáez L, Susanna A, Wikström N, Aldasoro JJ (2009) Reconstructing the history of Campanulaceae with a Bayesian approach to molecular dating and dispersal-vicariance analyses. Mol Phylogenet Evol 52:575–587

    PubMed  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seo H-S (2018) Population structure of Phedimus takesimensis (Crassulaceae) on Ulleung Island and molecular comparison with P. kamtschaticus, a continental progenitor. MS Thesis, Sungkyunkwan University, Korea

  • 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

    CAS  PubMed  Google Scholar 

  • Shetler SG, Morin N (1986) Seed morphology in North American Campanulaceae. Ann Missouri Bot Gard 73:653–688

    Google Scholar 

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

    Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sohn YK, Park KH (1994) Geology and evolution of Tok Island, Korea. J Geol Soc Korea 3:242–261

    Google Scholar 

  • Stevens PF (2001 onward) Angiosperm Phylogeny Website. Version 14, July 2017. https://www.mobot.org/MOBOT/research/APweb/

  • Stuessy TF, Ono M (1998) Evolution and speciation of island plants. Cambridge University Press, New York

    Google Scholar 

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

    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

    PubMed  Google Scholar 

  • Sun B-Y, 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

    Google Scholar 

  • Sun B-Y, Sul MR, Im JA, Kim CH, Kim TJ (2002) Evolution of endemic vascular plants of Ulleungdo and Dokdo in Korea-floristic and cytotaxonomic characteristics of vascular flora of Dokdo. Korean J Pl Taxon 32:143–158

    Google Scholar 

  • Sun B-Y, Shin H, Hyun J-O, Kim Y-D, Oh S-H (2014) Vascular plants of Dokdo and Ulleungdo Islands in Korea. The National Institute of Biological Resources, GeoBook Publishing Co, Korea

    Google Scholar 

  • Tackenberg O, Poschlod P, Bonn S (2003) Assessment of wind dispersal potential in plant species. Ecol Monogr 73:191–205

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Takayama K, Sun B-Y, 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

    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 (2015a) Genetic consequences of cladogenetic vs anagenetic speciation in endemic plants on oceanic islands. AoB Plants 7:plv102. https://doi.org/10.1093/aobpla/pvl102

    Article  PubMed  PubMed Central  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 (2015b) Relationships and genetic cosequences of contrasting modes of speciation among endemic species of Robinsonia (Asteraceae, Senecioneae) of the Juan Fernandez Archipelago, Chile, based on AFLPs and SSRs. New Phytol 205:415–428

    CAS  PubMed  Google Scholar 

  • Trusenkova OO, Stanichnyi SV, Ratner YB (2007) Major variability modes and wind patterns over the Sea of Japan and adjacent areas. Izv Atmos Ocean Phys 43:688–703

    Google Scholar 

  • Weiss H, Sun B-Y, Stuessy TF, Kim C-H, Kato H, Wakabayashi M (2002) Karyology of plant species endemic to Ulleung Island (Korea) and selected relatives in peninsular Korea and Japan. Bot J Linn Soc 138:93–105

    Google Scholar 

  • Yang J, Pak J-H, Maki M, Kim S-C (2019) Multiple origins and the population genetic structure of Rubus takesimensis (Rosaceae) on Ulleng Island: implications for the genetic consequences of anagenetic speciation. PLoS ONE 14:e0222707

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank two anonymous reviewers for their helpful comments and suggestions on an earlier version of the manuscript. This research was supported by the National Research Foundation of Korea (NRF-2016R1D1A2B03934596 and NRF-2019R1A2C2009841), to SCK.

Author information

Author notes

  1. Woo Young Cheong and Seon-Hee Kim contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, Sungkyunkwan University, 2066 Seobu-ro, Suwon, Gyeonggi-do, 16419, South Korea

    Woo Young Cheong, Seon-Hee Kim & Seung-Chul Kim

  2. School of Life Sciences, Research Institute for Dok-Do and Ulleung-Do Island, Kyungpook National University, 80 Daehak-ro, Bukgu, Daegu, 41566, South Korea

    JiYoung Yang, Woong Lee & Jae-Hong Pak

Authors
  1. Woo Young Cheong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seon-Hee Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. JiYoung Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Woong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jae-Hong Pak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seung-Chul Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WYC, SHK, JYY, and WL collected samples, and WYC and SHK generated and analyzed the data. JHP and SCK conceived the ideas and provided the overall direction for this project. The initial draft of this manuscript was written by WYC and subsequently edited by SCK. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Seung-Chul Kim.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 656 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheong, W.Y., Kim, SH., Yang, J. et al. Insights from Chloroplast DNA into the Progenitor-Derivative Relationship Between Campanula punctata and C. takesimana (Campanulaceae) in Korea. J. Plant Biol. 63, 431–444 (2020). https://doi.org/10.1007/s12374-020-09281-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09281-3

Keywords

Search

Navigation