Journal of Plant Research

, Volume 130, Issue 1, pp 107–116 | Cite as

Molecular phylogeny of the cosmopolitan aquatic plant genus Limosella (Scrophulariaceae) with a particular focus on the origin of the Australasian L. curdieana

  • Yu Ito
  • Norio Tanaka
  • Dirk C. Albach
  • Anders S. Barfod
  • Bengt Oxelman
  • A. Muthama Muasya
Regular Paper

Abstract

Limosella is a small aquatic genus of Scrophulariaceae of twelve species, of which one is distributed in northern circumpolar regions, two in southern circumpolar regions, two in the Americas, one endemic to Australia, and six in tropical or southern Africa or both. The Australasian L. curdieana has always been considered distinct but its close phylogenetic relationships have never been inferred. Here, we investigated the following alternative phylogenetic hypotheses based on comparative leaf morphology and habitat preferences or floral morphology: (1) L. curdieana is sister to the African L. grandiflora; or (2) it is closely related to a group of other African species and the northern circumpolar L. aquatica. We tested these hypotheses in a phylogenetic framework using DNA sequence data from four plastid DNA regions and the nuclear ITS region. These were analyzed using maximum parsimony and Bayesian inference. We obtained moderately resolved, partially conflicting phylogenies, supporting that accessions of L. grandiflora form the sister group to the rest of the genus and that L. curdieana groups with the African taxa, L. africana and L. major, and L. aquatica. Thus, the molecular evidence supports the second hypothesis. A biogeographic analysis suggests an out-of-southern Africa scenario and several dispersal events in the Southern Hemisphere. Past dispersal from southern Africa to Australasia is suggested, yet it cannot be excluded that a route via tropical Africa and temperate Asia has existed.

Keywords

Aquatic plants Biogeography Dispersal Lamiales Phylogenetic inference 

Supplementary material

10265_2016_872_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 17 kb)
10265_2016_872_MOESM2_ESM.docx (251 kb)
Supplementary material 2 (DOCX 251 kb)

References

  1. Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Mol Phylogenet Evol 1:3–16CrossRefPubMedGoogle Scholar
  2. Barker WR (1986) Limosella. In: Jessop JP, Toelken HR (eds) Flora of South Australia, vol 3., Polemoniaceae to compositeABRS/CISRO, Melbourne, pp 1282–1284Google Scholar
  3. Barker WR (1999) Limosella. In: Walsh NG, Entwisle TJ (eds) Flora of Victoria, vol 4., Dicotyledons cornaceae to asteraceaeInkata Press, Port Melbourne, pp 497–498Google Scholar
  4. Bell CD, Soltis DE, Soltis PS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97:1296–1303CrossRefPubMedGoogle Scholar
  5. Boere GC, Stroud DA (2006) The flyway concept: what it is and what it isn’t. In: Boere GC, Galbraith CA, Stroud DA (eds) Waterbirds around the world. The Stationery Office, Edinburgh, pp 40–47Google Scholar
  6. Brako L, Zarucchi JL (1993) Catalogue of the flowering plants and gymnosperms of Peru. Monographs in Systematic Botany volume 45, Missouri Botanical Garden, St. Louis, MOGoogle Scholar
  7. Cook CDK (2004) Aquatic and wetland plants of southern africa. Backhuys Publishers, LeidenGoogle Scholar
  8. Crisp MD, Cook LG (2013) How was the Australian Flora assembled over the last 65 million years? A molecular phylogenetic perspective. Annu Rev Ecol Evol Syst 44:303–324CrossRefGoogle Scholar
  9. Crow GE, Hellquist CB (2000) Limosella. In: Crow GE, Hellquist CB (eds) Aquatic and wetland plants of northeastern North America, vol 1., Pteridophytes, gymnosperms, and angiosperms: dicotyledonsThe University of Wisconsin Press, Madison, pp 327–329Google Scholar
  10. Darwin C (1872) The origin of species by means of natural selection. John Murray, LondonGoogle Scholar
  11. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–222CrossRefPubMedPubMedCentralGoogle Scholar
  12. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88CrossRefPubMedPubMedCentralGoogle Scholar
  13. Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319CrossRefGoogle Scholar
  14. Felsenstein J (1985) Confidence limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  15. Ghazanfar SA, Hepper FN, Philcox D (2008) Scrophulariaceae. In: Beentje HJ, Ghazanfar SA (eds) Flora of tropical East Africa. Published on behalf of the East African governments by Royal Botanic Gardens, Kew, UK, pp 1–211Google Scholar
  16. Glück K (1934) Novae species et varietates generis Limosellae. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem 12:71–78CrossRefGoogle Scholar
  17. Godfrey RK, Wooten JW (1981) Limosella. In: Godfrey RK, Wooten JW (eds) Aquatic and wetland plants of southeastern United States Dicotyledons. Univ Georgia Press, Athens, p 649Google Scholar
  18. Gorshkova SG (1997) Limosella L. In: Schischkin BK, Bobrow EG (eds) Flora of U.S.S.R. vol 22, pp 367–369Google Scholar
  19. Harden GJ (1992) Limosella. Flora of New South Wales, vol 3. New South Wales University Press, Australia, pp 563–564Google Scholar
  20. Heled J, Drummond A (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580CrossRefPubMedGoogle Scholar
  21. Hilliard OM, Burtt BL (1986) Notes on some plants of southern Africa chiefly from Natal: XII. Notes R Bot Gard Edinb 43:189–228Google Scholar
  22. Hong DY, Yang H, Jin CL, Holmgren NH (1998) Scrophulariaceae. In: Wu ZY, Raven PH (eds) Flora of China. Science Press, Beijing, pp 1–212Google Scholar
  23. 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. Am J Bot 97:1156–1167PubMedGoogle Scholar
  24. Ito Y, Tanaka N, García-Murillo P, Muasya AM (2016) A new delimitation of the Afro-Eurasian plant genus Althenia to include its Australasian relative, Lepilaena (Potamogetonaceae)—Evidence from DNA and morphological data. Mol Phylogenet Evol 98:261–270CrossRefPubMedGoogle Scholar
  25. Ivanina LI (2001) Limosella. In: Fedorov AA (ed) Flora of Russia, the European part and bordering regions, vol 5. A. A. Balkema, Rotterdam, pp 325–347Google Scholar
  26. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kokubugata G, Nakamura K, Forster PI, Hirayama Y, Yokota M (2012) Antitropical distribution of Lobelia species (Campanulaceae) between the Ryukyu Archipelago of Japan and Oceania as indicated by molecular data. Aust J Bot 60:417–428CrossRefGoogle Scholar
  28. Kornhall P, Bremer B (2004) New circumscription of the tribe Limoselleae (Scrophulariaceae) that includes the taxa of the tribe Manuleeae. Bot J Linn Soc 146:453–467CrossRefGoogle Scholar
  29. Little DP, Barrington DS (2003) Major evolutionary events in the origin and diversification of the fern genus Polystichum (Dryopteridaceae). Am J Bot 90:508–514CrossRefPubMedGoogle Scholar
  30. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, USA, pp 1–8Google Scholar
  31. Moore LB (1961) Limosella. In: Allan HH (ed) Flora of New Zealand, vol l., Government printerWellington, New Zealand, pp 846–847Google Scholar
  32. Moore TE, Verboom GA, Forest F (2010) Phylogenetics and biogeography of the parasitic genus Thesium L. (Santalaceae), with an emphasis on the Cape of South Africa. Bot J Linn Soc 162:435–452CrossRefGoogle Scholar
  33. Mort ME, Soltis DE, Soltis PS, Francisco-Ortega J, Santos-Guerra A (2001) Phylogenetic relationships and evolution of Crassulaceae inferred from matK sequence data. Am J Bot 88:76–91CrossRefPubMedGoogle Scholar
  34. Müller S, Salomo K, Salazar J, Naumann J, Jaramillo MA, Neinhuis C, Feild TS, Wanke S (2015) Intercontinental long-distance dispersal of Canellaceae from the New to the Old World revealed by a nuclear single copy gene and chloroplast loci. Mol Phylogenet Evol 84:205–219CrossRefPubMedGoogle Scholar
  35. Muńoz J, Felicisimo ÁM, Cabezas F, Burgaz AR, Martínez I (2004) Wind as a long- distance dispersal vehicle in the Southern Hemisphere. Science 304:1144–1147CrossRefPubMedGoogle Scholar
  36. Nakamura K, Denda T, Kokubugata G, Forster PI, Wilson GW, Peng C, Yokota M (2012) Molecular phylogeography reveals an antitropical distribution and local diversification of Solenogyne (Asteraceae) in the Ryukyu Archipelago of Japan and Australia. Biol J Linn Soc 105:197–217CrossRefGoogle Scholar
  37. Norup MF, Petersen G, Burrows S, Bouchenak-Khelladi Y, Leebens-Mack J, Pires JC, Linder HP, Seberg O (2015) Evolution of Asparagus L. (Asparagaceae): out-of-South-Africa and multiple origins of sexual dimorphism. Mol Phylogenet Evol 92:25–44CrossRefPubMedGoogle Scholar
  38. Nylander JAA (2002) MrModeltest v.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
  39. Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481CrossRefGoogle Scholar
  40. Oxelman B, Lidén M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst Evol 206:393–410CrossRefGoogle Scholar
  41. Oxelman B, Backlund M, Bremer B (1999) Relationships of the Buddlejaceae s. l. inferred from chloroplast rbcL and ndhF sequences. Syst Bot 24:164–182CrossRefGoogle Scholar
  42. Oxelman B, Komhall P, Olmstead RG, Bremer B (2005) Further disintegration of Scrophulariaceae. Taxon 54:411–425CrossRefGoogle Scholar
  43. Philcox D (1990) Limosella. In: Launert E, Pope GV (eds) Flora Zambesiaca, volume 8, part 2. Flora Zambesiaca Managing Committee, London, pp 73–75Google Scholar
  44. Rambaut A (2009) FigTree v1.3.1: Tree Figure Drawing Tool. http://tree.bio.ed.ac.uk/software/figtree/
  45. Rambaut A, Suchard MA, Xie W, Drummond AJ (2014) Tracer. Ver 1.6. http://beast.bio.ed.ac.uk/Tracer
  46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  47. 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 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rønsted N, Symonds MRE, Birkholm T, Christensen SB, Meerow AW, Molander M, Mølgaard P, Petersen G, Rasmussen N, van Staden J, Stafford GI, Jäger AK (2012) Can phylogeny predict chemical diversity and potential medicinal activity of plants? A case study of Amaryllidaceae. BMC Evol 12:182CrossRefGoogle Scholar
  49. Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b. Sinauer, Sunderland, Massachusetts, USAGoogle Scholar
  50. Taberlet P, Ludovic G, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefPubMedGoogle Scholar
  51. Webb DA (1972) Limosella. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea, vol 3, pp 205–216Google Scholar
  52. Wolf PG, Soltis PS, Soltis DE (1994) Phylogenetic relationships of Dennstaedtioid ferns: evidence from rbcL sequences. Mol Phylogenet Evol 3:383–392CrossRefPubMedGoogle Scholar
  53. Yamazaki T (1993) Limosella. In: Iwatsuki K, Yamazaki T, Boufford DE, Ohba H (eds) Flora of Japan, vol IIIa. Angiospermae Dicotyledoneae Sympetalae, Kodansha, p 334Google Scholar
  54. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724CrossRefPubMedGoogle Scholar
  55. Yu Y, Harris AJ, Blair C, He X (2015) RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol Phylogenet Evol 87:46–49CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  • Yu Ito
    • 1
    • 2
  • Norio Tanaka
    • 3
  • Dirk C. Albach
    • 4
  • Anders S. Barfod
    • 5
  • Bengt Oxelman
    • 6
  • A. Muthama Muasya
    • 7
  1. 1.Biological SciencesUniversity of CanterburyChristchurchNew Zealand
  2. 2.Xishuangbanna Tropical Botanical GardenThe Chinese Academy of SciencesKunmingPeople’s Republic of China
  3. 3.Tsukuba Botanical GardenNational Museum of Nature and ScienceTokyoJapan
  4. 4.Institute of Biology and Environmental Sciences (IBU)Carl von Ossietzky-University OldenburgOldenburgGermany
  5. 5.Department of BioscienceAarhus UniversityAarhus CDenmark
  6. 6.Department of Biological and Environmental SciencesUniversity of GothenburgGothenburgSweden
  7. 7.Department of Biological SciencesUniversity of Cape TownCape TownSouth Africa

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