Skip to main content

Advertisement

SpringerLink
Log in

Phylogeography of Cycas revoluta Thunb. (Cycadaceae) on the Ryukyu Islands: very low genetic diversity and geographical structure

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Variations in the chloroplast and mitochondrial DNA of Cycas revoluta Thunb. (Cycadaceae) were examined in 22 populations distributed across the Ryukyu Islands and southern Kyushu. Among the 14,130 bp of sequence examined, only one site mutation and one indel were polymorphic. The identified polymorphisms were located in the spacers between trnS (UGA) and trnfM (CAU) of the chloroplast DNA and between nad1 exon B and exon C of the mitochondrial DNA, respectively. Three haplotypes were identified from the Ryukyu Islands and southern Kyushu. The areas of distribution of the three haplotypes were highly geographically structured. The boundaries of two of the three haplotypes were demarcated by Okinoerabujima Island in the middle Ryukyus. The northern type and southern types lay north and south of the island, respectively. The third haplotype was almost sympatrically distributed with the southern type. The genetic variation within C. revoluta was estimated to be very low (h = 0.641, π = 0.00071) in comparison to its relative in Taiwan, C. taitungensis, which possesses 97 cpDNA haplotypes and 55 mtDNA haplotypes from two relic populations. A reasonable explanation for the low genetic diversity of the cycad on the Ryukyu Islands could be severe bottleneck effects, resulting from the submersion of low islands and the diminished landmass of islands in the interglacial age in the Quaternary period. The geographically restricted nature of the haplotypes could be attributed to vicariance resulting from the land configuration of the Ryukyu Islands, including changes in geography during the interglacial age in the Quaternary.

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

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Google Scholar 

  • Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803

    Article  CAS  Google Scholar 

  • Bremer K (1994) Branch support and tree stability. Cladistics 10:295–304

    Article  Google Scholar 

  • Chiang TY, Chiang YC, Chen YJ, Chou CH, Havanond S, Hong TN (2001) Phylogeography of Kandelia candel in east Asiatic mangroves based on nucleotide variation of chloroplast and mitochondrial DNAs. Mol Ecol 10:2697–2710

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Dehgan B, Yuen CKKH (1983) Seed morphology in relation to dispersal, evolution and propagation of Cycas L. Bot Gaz 144:412–418

    Article  Google Scholar 

  • Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic non-coding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    Article  CAS  PubMed  Google Scholar 

  • Farris JS (1970) Methods for computing Wagner trees. Syst Zool 19:83–92

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Fijii N, Ueda K, Watano Y, Shimizu T (1999) Further analysis of intraspecific sequence variation of chloroplast DNA in Primula cuneifolia Ledeb (Primuraceae): implications for biogeography of Japanese alpine flora. J Plant Res 112:87–95

    Article  Google Scholar 

  • Fujii N, Ueda K, Watano Y, Shimizu T (1995) Intraspecific sequence variation in chloroplast DNA of Primula cuneifolia Ledeb (Primuraceae). J Phytogeogr Taxon 43:15–24

    Google Scholar 

  • Fujii N, Ueda K, Watano Y, Shimizu T (1997) Intraspecific sequence variation of chloroplast DNA in Pedicularis chamissonis Steven (Scrophulariaceae) and geographic structuring of the Japanese “alpine” plants. J Plant Res 110:195–207

    Article  CAS  Google Scholar 

  • González-Astorga J, Vovides AP, Iglesias C (2003a) Morphological and geographic variation of the cycad Dioon edule Lindl (Zamiaceae): ecological and evolutionary implications. Bot J Linn Soc 141:465–470

    Article  Google Scholar 

  • González-Astorga J, Vovides AP, Ferrer MM, Iglesias C (2003b) Population genetics of Dioon edule Lindl (Zamiaceae, Cycadales): biogeographical and evolutionary implications. Biol J Linn Soc 80:457–467

    Article  Google Scholar 

  • González-Astorga J, Vergara-Silva F, Vovides AP, Nicolalde-Morejón F, Cabrera-Toledo D, Pérez-Farrera MA (2008) Diversity and genetic structure of three species of Dioon Lindl (Zamiaceae, Cycadales) from the Pacific seaboard of Mexico. Biol J Linn Soc 94:765–776

    Article  Google Scholar 

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    CAS  PubMed  Google Scholar 

  • Harris SA, Ingram R (1991) Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40:393–412

    Article  Google Scholar 

  • Hasebe M, Iwatsuki K (1990) Adiantum capillusveneris chloroplast DNA clone bank: as useful heterologous probes in the systematics of the leptosporangiate ferns. Am Fern J 80:20–25

    Article  Google Scholar 

  • Hayashi T, Matsui M (1988) Biochemical differentiation in Japanese newts, genus Cynops (Salamandridae). Zool Sci 5:1121–1126

    Google Scholar 

  • Hayashi T, Matsui M, Utsunomiya T, Tanaka S, Ota H (1992) Allozyme variation in the newt Tylototriton andersonii from three islands of the Ryukyu Archipelago. Herpetologica 48:178–184

    Google Scholar 

  • Hikida T, Motokawa J (1999) Phytogeographical relationships of the skinks of the genus Eumeces (Reptilia: Scincidae) in East Asia. In: Ota H (ed) Tropical island herpetofauna: origin current diversity and conservation tropical islands. Elsevier Science, Amsterdam, pp 231–247

    Google Scholar 

  • Hill KD (1996) Cycads in the Pacific. In: Keast A, Miller SE (eds) The origin and evolution of Pacific Islands biotas, New Guinea to eastern Polynesia: patterns and processes. Academic, Amsterdam, pp 267–274

    Google Scholar 

  • Hill KD (1999) Cycas–an evolutionary perspective. In: Chen CJ (ed) Biology and conservation of cycads. International Academic, Beijing, pp 98–115

    Google Scholar 

  • Hiramatsu M, Li K, Okubo H, Huang KL, Huang CW (2001) Biogeography and origin of Liliumu longiflorum and L. formosanum (Liliaceae) endemic to the Ryukyu Archipelago and Taiwan as determined by allozyme diversity. Am J Bot 88:1230–1239

    Article  CAS  PubMed  Google Scholar 

  • Hsieh HT (1999) Studies on population ecology and genetic variability of Cycas taitungensis. Master’s Thesis, Department of Biology, National Taiwan Normal University, Taipei

  • Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Hwang SY, Lin TP (2002) Spatial pattern of chloroplast DNA variation of Cyclobalanopsis glauca in Taiwan and East Asia. Mol Ecol 11:2349–2358

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583–589

    CAS  PubMed  Google Scholar 

  • Jian S, Zhong Y, Liu N, Gao Z, Wei Q, Xie Z, Ren H (2006) Genetic variation in the endangered endemic species Cycas fairylakea (Cycadaceae) in China and implications for conservation. Biodivers Conserv 15:1681–1694

    Article  Google Scholar 

  • Johnson LA, Soltis DE (1994) MatK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156

    Article  Google Scholar 

  • Jones DL (1993) Cycads of the world. Reed Books, Chatswood

    Google Scholar 

  • Kato J, Ota H, Hikida T (1994) Biochemical systematics of the Latiscutatus species-group of the genus Eumeces (Scincidae: Reptilia) from East Asian Islands. Biochem Syst Ecol 22:491–500

    Article  CAS  Google Scholar 

  • Keppel G, Lee SW, Hodgskiss PD (2002) Evidence for long isolation among populations of a Pacific cycads: genetic diversity and differentiation in Cycas seemannii A.Br. (Cycadaceae). J Hered 93:133–139

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1996) Quaternary paleogeography of the Ryukyu Arc. J Geogr 105:259–285

    Google Scholar 

  • Kimura M (2000) Paleogeography of the Ryukyu Islands. Tropics 10:5–24

    Article  Google Scholar 

  • Kizaki K (1985) Geology of the Ryukyu Arc. Okinawa Times, Naha

    Google Scholar 

  • Kizaki K, Oshiro I (1977) Palaeogeography of the Ryukyu Islands (in Japanese with English summary). Marine Sci Monthly 9:542–549

    Google Scholar 

  • Kizaki K, Oshiro I (1980) The origin of the Ryukyu Islands. In: Kizaki K (ed) Natural history of the Ryukyus (in Japanese). Tsukiji-shokan, Tokyo

    Google Scholar 

  • Maekawa K, Lo N, Kitade T, Miura T, Matsumoto T (1999) Molecular phylogeny and geographic distribution of wood-feeding cockroaches in east Asian islands. Mol Phyl Evol 13:360–376

    Article  CAS  Google Scholar 

  • Miikeda O, Yukawa T (2001) A simple procedure of DNA purification by gel filtration chromatography (in Japanese with English summary). Bunrui 1:79–82

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nei M, Tajima F (1983) Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105:205–217

    Google Scholar 

  • Osborne R, Stevenson DW, Hill KD (1999) The world list of cycads. In: Chen CJ (ed) Biology, conservation of cycads. International Academic, Beijing, pp 224–239

    Google Scholar 

  • Ota H (1998) Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Res Pop Ecol 40:189–204

    Article  Google Scholar 

  • Ota H (2000) The current geographic faunal pattern of reptiles and amphibians of the Ryukyu archipelago and adjacent regions. Tropics 10:51–62

    Article  Google Scholar 

  • Rozas J, Rozas R (1999) dnasp, Version 3.0: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175

    Article  CAS  PubMed  Google Scholar 

  • Setoguchi H, Ohba H (1995) Phylogenetic relationships in Crossostylis (Rhizophoraceae) inferred from restriction site variation of chloroplast DNA. J Plant Res 108:87–92

    Article  CAS  Google Scholar 

  • Setoguchi H, Watanabe I (2000) Intersectional gene flow between insular endemics in the genus Ilex (Aquifoliaceae) on the Bonin Islands and the Ryukyu Islands. Am J Bot 87:793–810

    Article  CAS  PubMed  Google Scholar 

  • Setoguchi H, Kyoda S, Maeda Y, Nomura N (2009) Geographical variation in leaflet of Cycas revoluta (Cycadaceae) on the Ryukyu Islands. J Phytogeogr Taxon 57:1–6

    Google Scholar 

  • Soltis DE, Soltis PS (1998) Choosing an approach and an appropriate gene for phylogenetic analysis. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II DNA sequencing. Kluwer Academic, Boston, pp 1–42

    Google Scholar 

  • Soltis DE, Soltis PS, Milligan BG (1992) Intraspecific chloroplast DNA variation: systematics and phylogenetic implication. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, New York, pp 117–150

    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 

  • Steel KP, Vilgalys R (1994) Phylogenetic analyses of Polemoniaceae using nucleotide sequences of the plastid gene matK. Syst Bot 19:126–142

    Article  Google Scholar 

  • Swofford DL (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Tanaka T, Matsui M, Takenaka O (1996) Phylogenetic relationships of Japanese brown frogs (Rana: Ranidae) assessed by mitochondrial cytochrome b gene sequences. Biochem Syst Ecol 24:299–307

    Article  CAS  Google Scholar 

  • Toda M (1999) Historical biogeography of East Asian populations of Rana limnocharis (Amphibia: Anura): a review. In: Ota H (ed) Tropical island herpetofauna: origin current diversity and conservation tropical islands. Elsevier Science, Amsterdam, pp 299–315

    Google Scholar 

  • Toda M, Nishida M, Tu M, Hikida T, Ohta H (1999) Genetic variation, phylogeny and biogeography of the pit vipers of the genus Trimeresurus sensu lato (reptilia: Viperidae) in the subtropical East Asian islands. In: Ota H (ed) Tropical island herpetofauna: origin current diversity and conservation tropical islands. Elsevier Science, Amsterdam, pp 249–270

    Google Scholar 

  • Treutlein J, Wink M (2002) Molecular phylogeny of cycads inferred from rbcL sequences. Naturwissenschaften 89:221–225

    Article  CAS  PubMed  Google Scholar 

  • Tsudzuki J, Nakashima K, Tsudzuki T, Hiratsuka J, Shibata M, Wakasugi T, Sugiura M (1993) Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: nucleotide sequences of trnQ, trnK, psbA, trnI and trnH and the absence of rps16. Mol Genome Genet 232:206–214

    Google Scholar 

  • Ujiie H (1990) Geological history of the Ryukyu Island Arc. In: Ujiie H (ed) Nature of Okinawa geomorphology and geology. Hirugisha, Naha, pp 251–255

    Google Scholar 

  • Yamazaki T (1995) Cycadaceae. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan, vol 1. Kodansha, Tokyo, p 263

    Google Scholar 

  • Yang SL, Merrow AW (1996) The Cycas pectinata (Cycadaceae) complex: genetic structure and gene flow. Int J Plant Sci 157:468–483

    Article  Google Scholar 

Download references

Acknowledgments

We thank Yoshiyuki Maeda (Hookaen), Junichi Nagasawa (Kyoto Botanical Garden), Zhou Zhekun (Kunming Institute of Botany, the Chinese Academy of Science), Ching I. Peng (Academia Sinica, Taiwan), K. Kaibe (Kyoto University), and the Forest Experiment Research Center at Kyoto University for providing cycad samples.

Author information

Authors and Affiliations

  1. Department of Biology, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, 606-8501, Japan

    S. Kyoda & Hiroaki Setoguchi

Authors
  1. S. Kyoda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroaki Setoguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroaki Setoguchi.

Appendix

Appendix

Table 5 presents information on the DNA regions examined and the respective primers.

Table 5 DNA regions examined and primers used in this study
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kyoda, S., Setoguchi, H. Phylogeography of Cycas revoluta Thunb. (Cycadaceae) on the Ryukyu Islands: very low genetic diversity and geographical structure. Plant Syst Evol 288, 177–189 (2010). https://doi.org/10.1007/s00606-010-0322-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-010-0322-1

Keywords

Search

Navigation