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Phylogeny of Sparganium (Typhaceae) revisited: non-monophyletic nature of S. emersum sensu lato and resurrection of S. acaule

Abstract

The diploid aquatic genus Sparganium (Typhaceae) comprises ca. 14 species mainly in cool temperate regions of the world. Among these, S. emersum comprises two infraspecific taxa, subspecies acaule from eastern North America and subspecies emersum from Eurasia and western North America (and occasionally from eastern North America as well). However, there has been some discussion regarding the monophyly of S. emersum sensu lato. We tested the hypothesis of a polyphyletic S. emersum sensu lato in a phylogenetic framework. Sequence data from six plastid DNA regions and nuclear phyC were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference. We obtained a moderately resolved phylogeny with the plastid DNA data set, while phylogenetically less-informative phyC was useful to distinguish morphological species and discern hybrid and non-hybrid specimens. Sparganium emersum sensu lato was resolved as polyphyletic, clustering with S. angustifolium and S. glomeratum, respectively. Sparganium acaule is resurrected to be a sister to S. glomeratum, for which synapomorphic and distinguishing morphological characters are provided. Three cases of hybridization were detected.

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References

  • Brayshaw TC (1985) Pondweeds and bur-reeds, and their relatives, of British Columbia. Occas Pap British Columbia Prov Mus Ser 26

  • Clarke LA, Rebelo CS, Gonçalves J, Boavida MG, Jordan P (2001) PCR amplification introduces errors into mononucleotide and dinucleotide repeat sequences. Molec Pathol 54:351–353

    CAS  Article  Google Scholar 

  • Cook CDK (1980) Sparganium. Flora Europaea, vol 5. Cambridge University Press, Cambridge, pp 274–275

    Google Scholar 

  • Cook CDK, Nicholls MS (1986) A monographic study of the genus Sparganium (Sparganiaceae). Part 1. Subgenus Xanthosparganium Holmberg. Bot Helv 96:213–267

    Google Scholar 

  • Cook CDK, Nicholls MS (1987) A monographic study of the genus Sparganium (Sparganiaceae): part 2. Subgenus Sparganium. Bot Helv 97:1–44

    Google Scholar 

  • Fay MF, Swensen SM, Chase MW (1997) Taxonomic affinities of Medusagyne oppositifolia (Medusagynaceae). Kew Bull 52:111–120

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ito Y, Ohi-Toma T, Murata J, Tanaka N (2010) Hybridization and polyploidy of an aquatic plant, Ruppia (Ruppiaceae), inferred from plastid and nuclear DNA phylogenies. Amer J Bot 97:1156–1167. doi:10.3732/ajb.0900168

    CAS  Google Scholar 

  • Kaul RB (1997) Sparganiaceae. In: Flora of North America Editorial Committee (ed) 1993+. Flora of North America North of Mexico, vol 22. Oxford University Press, New York, pp 270–277

    Google Scholar 

  • Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498

    Article  Google Scholar 

  • Kim C, Choi H-K (2011) Molecular systematics and character evolution of Typha (Typhaceae) inferred from nuclear and plastid DNA sequence data. Taxon 60:1417–1428

    Google Scholar 

  • Larson GE (1993) Aquatic and wetland vascular plants of the northern Great Plains, General Technical Report RM-238. US Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins

  • Little DP, Barrington DS (2003) Major evolutionary events in the origin and diversification of the fern genus Polystichum (Dryopteridaceae). Amer J Bot 90:508–514. doi:10.3732/ajb.90.3.508

    Article  Google Scholar 

  • Morong T (1888) Studies in the Typhaceae. II. Sparganium. Bull Torrey Bot Club 15:73–81

    Article  Google Scholar 

  • Nylander JAA (2002) MrModeltest. Ver 1.0. Program distributed by the author. Department of Systematic Zoology, Uppsala University, Uppsala. Available at: http://www.ebc.uu.se/systzoo/staff/nylander.html

  • Preston CD, Croft JM (1997) Aquatic plants in Britain and Ireland. Harley Books, Colchester

    Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer. Ver 1.6. Available at: http://beast.bio.ed.ac.uk/Tracer

  • Rieseberg LH (1991) Homoploid reticulate evolution in Helianthus: evidence from ribosomal genes. Amer J Bot 78:1218–1237

    Article  Google Scholar 

  • Rieseberg LH (1997) Hybrid origin of plant species. Annu Rev Ecol Syst 28:359–389. doi:10.1146/annurev.ecolsys.28.1.359

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    PubMed  PubMed Central  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    PubMed  CAS  Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771. doi:10.1080/10635150802429642

    PubMed  Article  Google Scholar 

  • Sulman JD, Drew BT, Drummond C, Hayasaka E, Systma KJ (2013) Systematics, biogeography, and character evolution of Sparganium (Typhaceae): diversification of a widespread aquatic lineage. Amer J Bot 100:2023–2039. doi:10.3732/ajb.1300048

    Article  Google Scholar 

  • Swofford DL (2002) PAUP: phylogenetic analysis using parsimony (and other methods). Ver 4.0b10. Sinauer Associates, Sunderland, USA

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882

    Article  Google Scholar 

  • Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis P, Soltis D, Doyle JJ (eds) Molecular systematics of plants II. Kluwer, Dordrecht, pp 265–296

    Chapter  Google Scholar 

  • Wendel JF, Stewart JM, Rettig J (1991) Molecular evidence for homoploid reticulate evolution among Australian species of Gossypium. Evolution 45:694–711

    Article  Google Scholar 

  • Whitten WM, Williams NH, Chase MW (2000) Subtribal and generic relationships of Maxillarieae (Orchidaceae) with emphasis on Stanhopeinae: combined molecular evidence. Amer J Bot 87:1842–1856

    CAS  Article  Google Scholar 

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Acknowledgments

The authors thank curators of the following herbaria for arranging loans from their institutions and/or for hospitality during our recent visits: J. Hall (ALTA), P. Catling (DAO), D. Boufford (GH), L. Lisitsyna (IBIW), A. Seregin (MW), B. Thiers, T. Zanoni (NY), and T. Dickinson (TRT); D. D. Sokoloff (Moscow), K. Shuto (FKSE), and K. Sawa (Yamagata) for providing Sparganium specimens; C. Ishii (Tsukuba) for help with DNA sequencing; and M. Sasagawa (Niigata) for help to collect samples. We would also like to thank H. Cota-Sanchez (SASK), J. Li (Kunming), J. Murata, H. Ikeda, and T. Ohi-Toma (TI) for their continuous encouragements and supports. This research was partly supported by Yamada Science Foundation Long-term Stay Abroad Program, Japan to YI, and JSPS KAKENHI Grant Number 25440224 to NT.

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Correspondence to Yu Ito.

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Ito, Y., Tanaka, N., Kim, C. et al. Phylogeny of Sparganium (Typhaceae) revisited: non-monophyletic nature of S. emersum sensu lato and resurrection of S. acaule . Plant Syst Evol 302, 129–135 (2016). https://doi.org/10.1007/s00606-015-1245-7

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  • DOI: https://doi.org/10.1007/s00606-015-1245-7

Keywords

  • Aquatic plants
  • Hybridization
  • Molecular phylogeny
  • phyC
  • Plastid DNA
  • Sparganium
  • Typhaceae