Abstract
Recent advances in phylogenetics indicate that reticulate evolution has played an important role in the emergence of Isoëtes species in the North Pacific region. However, the biogeographical origin of the North Pacific Isoëtes species remains contentious. We present a fossilcalibrated phylogeny of species from the North Pacific region based on molecular data. Within this framework, we discuss their ancestral areas and biogeographical history. North Pacific Isoëtes are divided into two clades: clade I, consisting of East Asian, Papua New Guinean, and Australian species, and clade II, consisting of West Beringian and western North American species. Within clade I, Australian Isoëtes species were an early divergent group, and Papua New Guinea’s species form a sister clade to the East Asian species. Biogeographical reconstructions suggest an Australasian origin for the East Asian species that arose through long-distance dispersal during the late Oligocene. Within clade II, I. asiatica from West Beringia forms a clade with I. echinospora and I. muricata from Alaska. Western North America was the area of origin for the dispersal of Isoëtes species to West Beringia via the Bering land bridge during the late Miocene. Our study identifies the biogeographic origin of the North Pacific Isoëtes and suggests long-distance dispersal as the most likely explanation for their intercontinental distribution.
Similar content being viewed by others
References
Akaike H (1974) A new look at the statistical model identification. IEEE T Automat Contr 19:716–723
Carlsen T, Elven R, Brochmann C (2010) The evolutionary history of Beringian Smelowskia (Brassicaceae) inferred from combined microsatellite and DNA sequence data. Taxon 59:427–438
Chen D-H, Ronald PC (1999) A rapid DNA minipreparation method suitable for AFLP and other PCR applications. Plant Mol Biol Rep 17:53–57
Chen L-Y, Chen J-M, Gituru BW, Wang Q-F (2012) Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol Biol 12:30
Choi H-K, Jung J, Kim C (2008) Two new species of Isoëtes (Isoëtaceae) from Jeju Island, South Korea. J Plant Biol 51:354–358
COSEWIC (2006) COSEWIC assessment and update status report on the Bolander’s quillwort Isoëtes bolanderi in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa
Cox CB, Moore PD (2010) Biogeography: an ecological and evolutionary approach. Ed 8, John Wiley and Sons, New Jersey
DeChine EG (2008) A bridge or a barrier? Beringia’s influence on the distribution and diversity of tundra plants. Plant Ecol Divers 1:197–207
Devos N, Vanderpoorten A (2009) Range disjunctions, speciation, and morphological transformation rates in the liverwort genus Leptocyphus. Evolution 63:779–792
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling tree. BMC Evol Biol 7:214
Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance in incongruence. Cladistics 10:315–319
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Gladenkov AY, Oleinik AE, Marincovich L, Barinov KB (2002) A refined age for the earliest opening of Bering Strait. Palaeogeogr Palaeoclimatol Palaeoecol 183:321–328
Havill NP, Campbell CS, Vining TF, LePage B, Bayer RJ, Donoghue MJ (2008) Phylogeny and biogeography of Tsuga (Pinaceae) inferred from nuclear ribosomal ITS and chloroplast DNA sequence data. Syst Bot 33:478–489
Hoot SB, Napier NS, Taylor WC (2004) Revealing unknown or extinct lineages within Isoëtes (Isoëtaceae) using DNA sequences from hybrids. Am J Bot 91:899–904
Hoot SB, Napier NS, Taylor WC (2006) Phylogeny and biogeography of Isoëtes (Isoëtaceae) based on nuclear and chloroplast DNA sequence data. Syst Bot 31:449–460
Jung J, Kim C, Kim H, Choi H-K (2009) Taxonomic examination of Isoëtes L. (Isoëtaceae) in South Korea. Korean J Plant Taxon 39: 63–73 (in Korean with English abstract)
Jung J, Ryu Y, Won H, Choi H-K (2013) Morphological and molecular characterization of a new record of Isoëtes coromandelina subsp. coromandelina from Cambodia. Plant Syst Evol 300:43–50
Kiefer C, Dobes C, Sharbel TF, Koch MA (2009) Phylogeographic structure of the chloroplast DNA gene pool in North American Boechera-A genus and continental-wide perspective. Mol Phylogenet Evol 52:303–311
Kim C, Bounphanmy S, Sun B-Y, Choi H-K (2010) Isoëtes laosiensis, a new species from Lao PDR. Am Fern J 100:45–53
Kim C, Na HR, Choi H-K (2009). Systematic evaluation of Isoëtes asiatica Makino (Isoëtaceae) based on AFLP, nrITS, and chloroplast DNA sequences. J Plant Biol 52:501–510
Kim C, Shin H, Chang Y-T, Choi H-K (2010). Speciation pathway of Isoëtes (Isoëtaceae) in East Asia inferred from molecular phylogenetic relationships. Am J Bot 97:958–969
Kim C, Shin H, Choi H-K (2009) Genetic diversity and population structure of diploid and polyploidy species of Isoëtes in East Asia based on AFLP markers. Int J Plant Sci 170:496–504
Kotoh K, Toh H (2008) Recent development in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298
Les DH, Crawford DJ, Kimball RT, Moody ML, Landolt E (2003) Biogeography of discontinuously distributed hydrophytes: A molecular appraisal of intercontinental disjunctions. Int J Plant Sci 164:917–932
Liu H, Wang Q-F, Taylor WC (2005) Isoëtes orientalis (Isoëtaceae), a new hexaploid quillwort from China. Novon 15:164–167
Liu X, Gituru WR, Wang Q-F (2004) Distribution of basic diploid and polyploidy species of Isoëtes in East Asia. J Geogr 31: 1239–1250
Marsden CR (1976) A new subspecies of Isoëtes coromandelina from Northern Australia. Contributions from Herbarium Australiense 24:1–10
Marsden CR (1979) Morphology and Taxonomy of Isoëtes in Australasia, India, North-East and South-East Asia, China, and Japan. Ph.D. thesis, University of Adelaide, Adelaide
Nelson G, Platnick NI (1981) Systematics and biogeography: cladistics and vicariance. Columbia University Press, New York
Nie Z-L, Wen J, Azuma H, Qiu Y-L, Sun H, Meng Y, Sun W-B, Zimmer EA (2008) Phylogenetic and biogeographic complexity of Magnoliaceae in the Northern Hemisphere inferred from three nuclear datasets. Mol Phylogenet Evol 48:1027–1040
Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (Are We There Yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583
Oliver C, Hollingsworth PM, Gornall RJ (2006) Chloroplast DNA phylogeography of the arctic-montane species Saxifraga hirculus (Saxifragaceae). Heredity 96:222–231
Perrie L, Brownsey P (2007) Molecular evidence for long-distance dispersal in the New Zealand pteridophyte flora. J Geogr 34: 2028–2038
Pigg KB (2001) Isoetalean lycopsid evolution: from the Devonian to the present. Am Fern J 91:99–114
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Qiu Y-X, Sun Y, Zhang X-P, Lee J, Fu C-X, Comes HP (2009) Molecular phylogeography of East Asian Kirengeshoma (Hydrangeaceae) in relation to Quaternary climate change and landbridge configurations. New Phytol 183:480–495
Rambaut A, Drummond AJ (2003) Tracer, ver. 1.5. 2003. Available from http://tree.bio.ed.ac.uk/software/Tracer/
Retallack GJ (1997) Earliest Triassic origin of Isoëtes and quillwort evolutionary radiation. J Paleontol 71:500–521
Ronquist F, Huelsenbeck JP (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Sclater JG, Fisher RL (1974) The evolution of the east central Indian Ocean, with emphasis of the tectonic setting of the Ninetyeast Ridge. Geol Soc Am Bull 85:683–702
Sheahan MC, Chase MW (2000) Phylogenetic relationships within Zygophyllaceae based on DNA sequences of three plastid regions, with special emphasis on Zygophylloideae. Syst Bot 25: 371–384
Skog JE, Dilcher DL, Potter FW (1992) A new species of Isoëtites from the mid-Cretaceous Dakota group of Kansas and Nebraska. Am Fern J 82:151–161
Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), ver. 4.0b10. Sinauer Associates, Sunderland
Takamiya M (1999) Natural history and taxonomy of Isoëtes (Isoëtaceae). Acta Phytotaxonomica Geobotanica 50:101–138 (in Japanese)
Takamiya M, Watanabe M, Ono K (1997) Biosystematic studies on the genus Isoëtes (Isoëtaceae) in Japan. IV. Morphology and anatomy of sporophytes, phytogeography and taxonomy. Acta Phytotaxonomica Geobotanica 48:89–122
Taylor WC, Hickey RJ (1992) Habitat, evolution and speciation in Isoëtes. Ann Mo Bot Gard 79:613–622
Taylor WC, Lekschas AR, Wang QF, Liu X, Napier NS, Hoot SB (2004) Phylogenetic relationships of Isoëtes (Isoëtaceae) in China as revealed by nucleotide sequences of the nuclear ribosomal ITS region and the second intron of a LEAFY homolog. Am Fern J 94:196–205
Taylor WC, Luebke NT, Britton DM, Hickey RJ, Brunton DF (1993) Isoëtaceae Reichenbach. In: FNA Editorial Committee (eds) Flora of North America: pteridophytes and gymnosperms, vol. 2. Oxford University Press, New York, pp 64–75
Taylor WC, Wagner WH, Hobdy RW, Warshauer FR (1993) Isoëtes hawaiiensis: a previously undescribed quillwort from Hawaii. Am Fern J 83:67–70
Tiffney BH (1985) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J Arnold Arboretum 66:73–94
Tkach N, Hoffmann MH, Roeser M, Korobkov AA, Von Hagen KB (2008) Parallel evolutionary patterns in multiple lineages of arctic Artemisia L. (Asteraceae). Evolution 62:184–198
Troia A (2001) The genus Isoëtes L. (Lycophyta, Isoëtaceae): synthesis of karyological data. Webbia 56:201–218
Tryon R (1986) The biogeography of species, with special reference to ferns. Bot Rev 52:117–156
Vanderpoorten, A, Gradstein SR, Carine MA, Devos N (2010) The ghosts of Gondwana and Laurasia in modern liverwort distributions. Biol Rev 85:471–487
Wang Q-F, Liu X, Taylor WC, He Z-R (2002) Isoëtes yunguiensis (Isoëtaceae), a new basic diploid quillwort from China. Novon 12:587–591
Wen J, Ickert-Bond SM, Nie ZL, Li R (2010) Timing and modes of evolution of eastern Asia-North American biogeographic disjunctions in seed plant. In: Long M, Gu H, Zhou Z, eds, Darwin’s heritage today: Proceeding of the Darwin 200 Beijing International Conference. Higher Education Press, Beijing, pp 252–269
White TJ, Birns T, Lee S, Taylor J (1999) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: A guide to methods and applications, Academic Press, New York, pp 315–322
Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Phylogenet Evol 14:717–724
Yu H, Nason JD, Ge X, Zeng J (2010) Slatkin’s Paradox: when direct observation and realized gene flow disagree. A case study in Ficus. Mol Ecol 19:4441–4453
Yu Y, Harris AJ, Blair C, He XJ (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol 87:46–49
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Kim, C., Choi, HK. Biogeography of North Pacific Isoëtes (Isoëtaceae) inferred from nuclear and chloroplast DNA sequence data. J. Plant Biol. 59, 386–396 (2016). https://doi.org/10.1007/s12374-016-0123-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-016-0123-3