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Genetic evidence of the southward founder speciation of Cycas taitungensis from ancestral C. revoluta along the Ryukyu Archipelagos

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Abstract

Cycas taitungensis and its sister species, C. revoluta (Cycas sect. Asiorientalis), are distributed peripatrically. Previous studies have revealed their phylogeographic pattern and, based on certain plastid DNA markers, have established that they diverged recently. However, the speciation process involving the genomic divergence has not been well clarified. In this study, based on their geographical distribution and estimates of their genetic diversity, two speciation models are proposed: (1) the founder and (2) the bottleneck speciation mode. Using approximate Bayesian computation (ABC) in combination with their estimated genetic diversity and population structure, we infer that the ancestral C. taitungensis populations diverged and southward colonized southeastern Taiwan from ancestral C. revoluta since the middle Pleistocene. These founders preserved ancestral polymorphism, resulting in small differences in genetic diversity and effective population size (Ne), despite a large difference in census population size (Nc) between two species. Based on this case of island cycad species offshore of continental Asia, this study provides new insight into how the speciation process influences the genetic diversity pattern of species with small Nc and Ne.

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References

  • Antao T, Beaumont MA (2011) Mcheza: a workbench to detect selection using dominant markers. Bioinformatics 27:1717–1718

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B (2009) Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205

    Article  CAS  PubMed  Google Scholar 

  • Chen M-P, Huang C-K, Lo L, Wang C-H (1992) Late Pleistocene paleoceanography of the Kuroshio Current in the area offshore Southeast Taiwan. Terr Atmos Ocean Sci 3:81–110

    Article  Google Scholar 

  • Chiang T-Y, Schaal BA (2006) Phylogeography of plants in Taiwan and the Ryukyu archipelago. Taxon 55:31–41

    Article  Google Scholar 

  • Chiang Y-C, Hung K-H, Moore S-J, Ge X-J, Huang S, Hsu T-W, Schaal BA, Chiang T (2009) Paraphyly of organelle DNAs in Cycas Sect. Asiorientales due to ancient ancestral polymorphisms. BMC Evol Bio 9:161

    Article  CAS  Google Scholar 

  • Chiang Y-C, Huang B-H, Liao P-C (2012) Diversification, biogeographic pattern, and demographic history of Taiwanese Scutellaria species inferred from nuclear and chloroplast DNA. PLoS ONE 7:e50844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang T-Y, Chen S-F, Kato H, Hwang C-C, Moore S-J, Hsu T-W, Hung K-H (2014) Temperate origin and diversification via southward colonization in Fatsia (Araliaceae), an insular endemic genus of the West Pacific Rim. Tree Genet Genomes 10:1317–1330

    Article  Google Scholar 

  • Condamine FL, Nagalingum NS, Marshall CR, Morlon H (2015) Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior in Bayesian molecular dating. BMC Evol Biol 15:65

    Article  PubMed  PubMed Central  Google Scholar 

  • Daruka I, Ditlevsen PD (2015) A conceptual model for glacial cycles and the middle Pleistocene transition. Clim Dyn 46:29–40

    Article  Google Scholar 

  • Doyle J (1991) DNA protocols for plants. In: Molecular techniques in taxonomy, vol 57. Springer, Switzerland, pp 283–293

    Chapter  Google Scholar 

  • Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R, Briscoe DA, Ballou JD (2010) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Garb JE, Gillespie RG (2009) Diversity despite dispersal: colonization history and phylogeography of Hawaiian crab spiders inferred from multilocus genetic data. Mol Ecol 18:1746–1764

    Article  CAS  PubMed  Google Scholar 

  • Hall R (2009) Southeast Asia’s changing palaeogeography. Blumea 54:148–161

    Article  Google Scholar 

  • Head MJ, Gibbard PL (2015) Early-Middle Pleistocene transitions: linking terrestrial and marine realms. Quat Int 389:7–46

    Article  Google Scholar 

  • Hsiung HY, Huang BH, Chang JT, Huang YM, Huang CW, Liao PC (2017) Local climate heterogeneity shapes population genetic structure of two undifferentiated insular Scutellaria Species. Front Plant Sci 8:159

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsu S-K, Sibuet J-C (1995) Is Taiwan the result of arc-continent or arc-arc collision? EPSL 136:315–324

    Article  CAS  Google Scholar 

  • Hu A, Meehl GA, Otto-Bliesner BL, Waelbroeck C, Han W, Loutre M-F, Lambeck K, Mitrovica JX, Rosenbloom N (2010) Influence of Bering Strait flow and North Atlantic circulation on glacial sea-level changes. Nat Geosci 3:118–121

    Article  CAS  Google Scholar 

  • Huang S, Chiang Y-C, Schaal BA, Chou C-H, 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, Hsieh HT, Fang K, Chiang YC (2004) Patterns of genetic variation and demography of Cycas taitungensis in Taiwan. Bot Rev 70:86–92

    Article  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 

  • Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602

    Article  PubMed  Google Scholar 

  • Jeffreys H (1998) The theory of probability. OUP, Oxford

    Google Scholar 

  • Juan C, Emerson BC, Oromı́ P, Hewitt GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends Ecol Evol 15:104–109

    Article  CAS  PubMed  Google Scholar 

  • Kawai K, Terada R, Kuwahara S, Takarabe M, Nishimura A, Hatta A, Hayward P, Yamamoto S, Takezaki T, Niimura H (2013) The Islands of Kagoshima: culture, society, industry and nature. Kagoshima University Research Center for the Pacific Islands, Kagoshima

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyoda S, Setoguchi H (2010) Phylogeography of Cycas revoluta Thunb. (Cycadaceae) on the Ryukyu Islands: very low genetic diversity and geographical structure. Plant Syst Evol 288:177–189

    Article  Google Scholar 

  • Lariushin B (2013) Cycadaceae family, 1st edn. CreateSpace Independent Publishing Platform, Scotts Valley

    Google Scholar 

  • Laval G, Excoffier L (2004) SIMCOAL 2.0: a program to simulate genomic diversity over large recombining regions in a subdivided population with a complex history. Bioinformatics 20:2485–2487

    Article  CAS  PubMed  Google Scholar 

  • Luis D, Gómez P (1994) Cycads of the world. Ancient plants in today’s landscape. Econ Bot 48:34

    Article  Google Scholar 

  • Mayr E (1982) Speciation and macroevolution. Evolution 36:1119–1132

    Article  PubMed  Google Scholar 

  • Nagalingum N, Marshall C, Quental T, Rai H, Little D, Mathews S (2011) Recent synchronous radiation of a living fossil. Science 334:796–799

    Article  CAS  PubMed  Google Scholar 

  • Norstog K, Nicholls TJ (1997) The biology of the cycads. Cornell University Press, Ithaca

    Google Scholar 

  • Osozawa S, Shinjo R, Armid A, Watanabe Y, Horiguchi T, Wakabayashi J (2012) Palaeogeographic reconstruction of the 1.55 Ma synchronous isolation of the Ryukyu Islands, Japan, and Taiwan and inflow of the Kuroshio warm current. Int Geol Rev 54:1369–1388

    Article  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 Popul Ecol 40:189–204

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu YX, Fu CX, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world’s most diverse temperate flora. Mol Phylogenet Evol 59:225–244

    Article  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Resour 4:137–138

    Article  Google Scholar 

  • Salas-Leiva DE, Meerow AW, Calonje M, Griffith MP, Francisco-Ortega J, Nakamura K, Stevenson DW, Lewis CE, Namoff S (2013) Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony, likelihood and species tree inference methods. Ann Bot 112:1263–1278

    Article  PubMed  PubMed Central  Google Scholar 

  • Sexton JP, Hangartner SB, Hoffmann AA (2014) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68:1–15

    Article  CAS  PubMed  Google Scholar 

  • Sfenthourakis S, Triantis KA (2017) The Aegean archipelago: a natural laboratory of evolution, ecology and civilisations. J Biol Res Thessalon 24:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Sibuet J-C, Hsu S-K (1997) Geodynamics of the Taiwan arc-arc collision. Tectonophysics 274:221–251

    Article  Google Scholar 

  • Sibuet J-C, Hsu S-K (2004) How was Taiwan created? Tectonophysics 379:159–181

    Article  Google Scholar 

  • Su Y-C, Brown RM, Chang Y-H, Lin C-P, Tso IM (2016) Did a Miocene-Pliocene island isolation sequence structure diversification of funnel web spiders in the Taiwan-Ryukyu Archipelago? J Biogeogr 43:991–1003

    Article  Google Scholar 

  • Team RC (2015) R: a language and environment for statistical computing. https://www.R-project.org/

  • Templeton AR (2008) The reality and importance of founder speciation in evolution. BioEssays 30:470–479

    Article  PubMed  Google Scholar 

  • Thieret JW (1958) Economic botany of the cycads. Econ Bot 12:3–41

    Article  Google Scholar 

  • Tseng H-Y, Huang W-S, Jeng M-L, Villanueva RJT, Nuñeza OM, Lin C-P (2018) Complex inter-island colonization and peripatric founder speciation promote diversification of flightless Pachyrhynchus weevils in the Taiwan-Luzon volcanic belt. J Biogeogr 45:89–100

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Tvd Lee, Hornes M, Friters A, Pot J, Paleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Dai J, Zhao X, Li Y, Graham SA, He D, Ran B, Meng J (2014) Outward-growth of the Tibetan Plateau during the Cenozoic: a review. Tectonophysics 621:1–43

    Article  Google Scholar 

  • Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L (2010) ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinform 11:116

    Article  CAS  Google Scholar 

  • Whitelock LM (2002) The cycads. Timber Press, Portland

    Google Scholar 

  • Yang Y-Q, Huang B-H, Yu Z-X, Liao P-C (2015) Inferences of demographic history and fine-scale landscape genetics in Cycas panzhihuaensis and implications for its conservation. Tree Genet Genomes 11:78

    Article  Google Scholar 

  • Zheng Y, Liu J, Feng X, Gong X (2017) The distribution, diversity, and conservation status of Cycas in China. Ecol Evol 7:3212–3224

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Chung-Wei You for his helpful sampling of C. revoluta among the Ryukyu Islands. We thank the National Center for Genome Medicine of the National Core Facility Program for Biotechnology, Ministry of Science and Technology, Taiwan, for technical and bioinformatics support. We acknowledge Chih-Chieh Yu and Hsiao-Lei Liu for the suggestion of contents. We also thank Dr. Hubert Turner for English editing of the manuscript. This research was financially supported by the Ministry of Science and Technology of Taiwan (Grant Number: MOST 105–2628-B-003–001-MY3 and MOST 105–2628-B-003–002-MY3) and was also subsidized by National Taiwan Normal University (NTNU), Taiwan.

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Authors and Affiliations

  1. School of Life Science, National Taiwan Normal University, No. 88, Sec. 4, Ting-chow Rd., Wenshan Dist. 116, Taipei City, Taiwan

    Jui-Tse Chang, Bing-Hong Huang & Pei-Chun Liao

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  1. Jui-Tse Chang
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Contributions

JTC and PCL conceived the project and collected field samples. JTC conducted genetic experiments, performed statistical analyses, interpreted the data, and wrote the manuscript. BHH assisted in the genetic diversity and evolutionary analyses. PCL critically reviewed the draft. All authors read and approved the final manuscript.

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Correspondence to Pei-Chun Liao.

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10592_2019_1193_MOESM1_ESM.tif

Supplementary material 1 (TIFF 93 kb) Supplementary Fig. 1 Isolation by distance (IBD) result by Mantel test. The pairwise correlation between genetic and geographical distance shows the non-significant result.

Supplementary material 2 (TIFF 146 kb) Supplementary Fig. 2 The ln(K) and delta K plots.

10592_2019_1193_MOESM3_ESM.tif

Supplementary material 3 (TIFF 689 kb) Supplementary Fig. 3 The population structure analysis from K = 5 to K = 10 with 1 million MCMC times and 10% burn-in.

10592_2019_1193_MOESM4_ESM.docx

Supplementary material 4 (DOCX 21 kb) Supplementary Table 1. The prior setting of two evolutionary scenarios. A) Bottleneck hypothesis B) Founder hypothesis. Ne, rel, m, GAMMA and rec refer to the effective population size, relative rate, migration rate, gamma distribution (for estimating recombination and mutation rate) and recombination rate.

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Chang, JT., Huang, BH. & Liao, PC. Genetic evidence of the southward founder speciation of Cycas taitungensis from ancestral C. revoluta along the Ryukyu Archipelagos. Conserv Genet 20, 1045–1056 (2019). https://doi.org/10.1007/s10592-019-01193-1

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