Advertisement

Journal of Plant Research

, Volume 132, Issue 3, pp 335–344 | Cite as

Molecular phylogenetic species delimitation in the aquatic genus Ottelia (Hydrocharitaceae) reveals cryptic diversity within a widespread species

  • Yu ItoEmail author
  • Norio Tanaka
  • Anders S. Barfod
  • Josef Bogner
  • Jie Li
  • Okihito Yano
  • Stephan W. Gale
Regular Paper

Abstract

Ottelia, a pantropical genus of aquatic plants belonging to the family Hydrocharitaceae, includes several narrowly distributed taxa in Asia. Although the Asian species have received comparatively more research attention than congeners in other areas, various key taxonomic questions remain unaddressed, especially with regards to apparent cryptic diversity within O. alismoides, a widespread species complex native to Asia, northern Australia and tropical Africa. Here we test taxonomic concepts and evaluate species boundaries using a phylogenetic framework. We sampled five of the seven species of Ottelia in Asia as well as each species endemic to Africa and Australia; multiple samples of O. alismoides were obtained from across Asia. Phylogenetic trees based on five plastid DNA markers and the nuclear ITS region shared almost identical topologies. A Bayesian coalescent method of species delimitation using the multi-locus data set discerned one species in Africa, one in Australia and four in Asia with the highest probability. The results lead us to infer that a population sampled in Thailand represents a hitherto unrecognised cryptic taxon within the widespread species complex, although the apparent lack of unambiguous diagnostic characters currently precludes formal description. Conversely, no molecular evidence for distinguishing O. cordata and O. emersa was obtained, and so the latter is synonymised under the former. Two accessions that exhibit inconsistent positions among our phylogenetic trees may represent cases of chloroplast capture, however incomplete lineage sorting or polyploidy are alternative hypotheses that ought to be tested using other molecular markers.

Keywords

Alismatales Indo-Burma Biodiversity Hotspot Monocotyledons New species Species delimitation STACEY 

Notes

Acknowledgements

The authors thank H. Wang (HITBC) and E. Liu (KUN) for arranging loans from their institutions and/or for hospitality during the authors’ recent visits; R. Pooma, S. Saengrit, N. Suphuntee, K. Chayamarit (BKF), K. Shuto (Fukushima), S.R. Yadav (Shivaji), H. Murata (Osaka), T. Sugawara (MAK), Nb. Tanaka (TNS), J. Murata, T. Ohi-Toma (TI), A. Naiki, Y. Saito (Okinawa) for assistance in the field; and C. Ishii (Tsukuba) for help with DNA sequencing. This research was supported by Chinese Academy of Sciences (CAS) President’s International Fellowship Initiative (PIFI) Grant no. 2015PB022 to YI and by the ‘Integrated analysis of natural history collections for conservation of highly endangered species’ programme under the National Museum of Nature and Science, Japan to NT.

Supplementary material

10265_2019_1109_MOESM1_ESM.pdf (244 kb)
Supplementary material 1 (PDF 243 kb)

References

  1. Angulo A, Icochea J (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Syst Biodiv 8:357–370CrossRefGoogle Scholar
  2. Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the Compositae. Mol Phylogenet Evol 1:3–16CrossRefGoogle Scholar
  3. Bouckaert RR, Heled J, Kühnert D, Vaughan TG, Wu C-H, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537CrossRefGoogle Scholar
  4. Chase MW, Cowan RS, Hollingsworth PM, van den Berg C, Madriñan S, Petersen G, Seberg O, Jørgsensen T, Cameron KM, Carine M, Pedersen N, Hedderson TAJ, Conrad F, Salazar GA, Richardson JE, Hollingsworth ML, Barraclough TE, Kelly L, Wilkinson M (2007) A proposal for a standardised protocol to barcode all land plants. Taxon 56:295–299CrossRefGoogle Scholar
  5. Chen LY, Chen JM, Gituru RW, Wang QF (2012) Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol Biol 12:30CrossRefGoogle Scholar
  6. Cook CDK (1996) Aquatic and wetland plants of India. Oxford University, OxfordGoogle Scholar
  7. Cook CDK, Urmi-König K (1984) A revision of the genus Ottelia (Hydrocharitaceae). 2. The species of Eurasia, Australasia and America. Aquat Bot 20:131–177CrossRefGoogle Scholar
  8. Cook CDK, Symoens J-J, Urmi-König K (1983) A revision of the genus Ottelia (Hydrocharitaceae). 1. Generic considerations. Aquat Bot 18:263–274CrossRefGoogle Scholar
  9. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24:332–340CrossRefGoogle Scholar
  10. den Hartog C (1957) Hydrocharitaceae. In: van Steenis CGGJ (ed) Flora Malesiana, ser. 1, vol 5. Noordhoff-Kollf. Djakarta, pp 381 − 413Google Scholar
  11. Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–222CrossRefGoogle Scholar
  12. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88CrossRefGoogle Scholar
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  14. Funk WC, Caminer M, Ron SR (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proc R Soc B 279:1806–1814CrossRefGoogle Scholar
  15. Govaerts R (2018) World checklist of Hydrocharitaceae. Facilitated by the royal botanic gardens, Kew. Published online at http://apps.kew.org/wcsp/. Retrieved 22 December 2018
  16. Haynes RR (2001) Hydrocharitaceae. In: Santisuk T, Larsen K (eds) Flora of Thailand, vol 7. The Forest Herbarium. Royal Forest Department, Bangkok, pp 365–382Google Scholar
  17. He J-B, Sun X-Z (1990) Ottelia emersa Z.C. Zhao et R.L. Luo (Hydrocharitaceae)—a Synonym of O. cordata (Wallich) Dandy. Aquat Bot 36:395–398CrossRefGoogle Scholar
  18. He J-B, Sun X-Z, Wang H-Q (1990) Taxonomy of the bisexual species of Ottelia in China. Aquat Bot 36:389–393CrossRefGoogle Scholar
  19. Hutchinson J, Dalziel JM (1958) Flora of west tropical Africa vol. I. part 2 (2nd edn revised by Keay RWJ). Royal Botanic Gardens, Kew, pp 1662–1664Google Scholar
  20. 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 97:1156–1167CrossRefGoogle Scholar
  21. Ito Y, Tanaka N, Albach DC, Barfod AS, Oxelman B, Muasya AM (2017) Molecular phylogeny of the cosmopolitan aquatic plant genus Limosella (Scrophulariaceae) with a particular focus on the origin of the Australasian L. curdieana. J Plant Res 140:107–116CrossRefGoogle Scholar
  22. Jacobs SWL, McColl KA (2011) Hydrocharitaceae. In: Wilson AJG (ed) Flora of Australia, vol 39. ABRS/CSIRO, Melbourne, pp 14–44Google Scholar
  23. Johnson LA, Soltis DE (1998) Assessing congruence: empirical examples from molecular data. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematic of plants II: DNA sequencing. Kluwer Academic Publisher, Norwell, pp 265–296Google Scholar
  24. Jones GL (2017) Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J Math Biol 74:447–467CrossRefGoogle Scholar
  25. Jones GL, Aydin Z, Oxelman B (2015) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31:991–998CrossRefGoogle Scholar
  26. Juffe-Bignoli, D (2011) Ottelia cordata. The IUCN red list of threatened species 2011: e.T194035A8879309. http://dx.doi.org/10.2305/IUCN.UK.2011-2.RLTS.T194035A8879309.en. Downloaded on 09 January 2019
  27. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefGoogle Scholar
  28. Les DH, Tippery NP (2013) In time and with water. the systematics of alismatid monocotyledons. In: Wilkin P, Mayo SJ (eds) Early events in monocot evolution. Cambridge University Press, Cambridge, pp 119–164Google Scholar
  29. Les DH, Cleland MA, Waycott M (1997) Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (‘seagrasses’) and hydrophily. Syst Bot 22:443–463CrossRefGoogle Scholar
  30. Les DH, Moody ML, Soros C (2006) A reappraisal of phylogenetic relationships in the monocotyledon family Hydrocharitaceae. In: Columbus JT, Friar EA, Porter JM, Prince LM, Simpson MG (eds) Monocots: comparative biology and evolution: excluding Poales. Rancho Santa Ana Botanical Garden, Claremont, pp 211–230Google Scholar
  31. Little DP, Barrington DS (2003) Major evolutionary events in the origin and diversification of the fern genus Polystichum (Dryopteridaceae). Am J Bot 90:508–514CrossRefGoogle Scholar
  32. Lohman DJ, Ingram KK, Prawiradilaga DM, Winker K, Sheldon FH, Moyle RG, Ng PKL, Ong PS, Wang LK, Braile TM, Astuti D, Meier R (2010) Cryptic diversity in “widespread” southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biol Conserv 143:1885–1890CrossRefGoogle Scholar
  33. Luo RL, Wang HQ (1987) A new species of Ottelia (Hydrocharitaceae) and its karyotype. J Wuhan Bot Res 5:339–342Google Scholar
  34. Manthey JD, Klicka J, Spellman GM (2011) Cryptic diversity in a widespread North American songbird: phylogeography of the Brown Creeper (Certhia americana). Mol Phylogenet Evol 58:502–512CrossRefGoogle Scholar
  35. McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme Van Reine WF, Smith GF, Wiersema JH, Turland NJ (eds) (2012) International code of nomenclature for algae, fungi and plants (Melbourne Code): Adopted by the Eighteenth International Botanical Congress, Melbourne, Australia, July 2011. Regnum Vegetabile 154. Koeltz Scientific Books, KönigsteinGoogle Scholar
  36. 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, pp 1–8. http://www.phylo.org/sub_sections/portal/cite.php
  37. Nylander JAA (2002) MrModeltest. Ver. 1.0. Program distributed by the author. Department of Systematic Zoology, Uppsala University, Uppsala. Retrieved from http://www.ebc.uu.se/systzoo/staff/nylander.html
  38. Oliver PM, Adams M, Lee MSY, Hutchinson MN, Doughty P (2009) Cryptic diversity in vertebrates: molecular data double estimates of species diversity in a radiation of Australian lizards (Diplodactylus, Gekkota). Proc R Soc B 276:2001–2007CrossRefGoogle Scholar
  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, Backlund M, Bremer B (1999) Relationships of the Buddlejaceae s. l. inferred from chloroplast rbcL and ndhF sequences. Syst Bot 24:164–182CrossRefGoogle Scholar
  41. Phiri EE, Daniels SR (2016) Multilocus coalescent species delimitation reveals widespread cryptic differentiation among Drakensberg mountain-living freshwater crabs (Decapoda: Potamonautes). Invertebr Syst 30:60–74CrossRefGoogle Scholar
  42. Rambaut A (2009) FigTree ver. 1.3.1: Tree Figure Drawing Tool. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
  43. Rambaut A, Suchard MA, Xie W, Drummond AJ (2014) Tracer. ver. 1.6. Retrieved from http://beast.bio.ed.ac.uk/Tracer
  44. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  45. 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 61:539–542CrossRefGoogle Scholar
  46. Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51:492–508CrossRefGoogle Scholar
  47. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefGoogle Scholar
  48. Swofford DL (2002) PAUP: Phylogenetic analysis using parsimony (and other methods). ver. 40b10. Sinauer Associates, SunderlandGoogle Scholar
  49. Tanaka N (2015) Hydrocharitaceae. In: Ohashi H, Kadota Y, Murata J, Yonekura K, Kihara H (eds) Wild flowers of Japan, vol 1. Heibonsha, Tokyo, pp 118–125 (in Japanese) Google Scholar
  50. Tanaka N, Setoguchi H, Murata J (1997) Phylogeny of the family Hydrocharitaceae inferred from rbcL and matK gene sequence data. J Plant Res 110:329–337CrossRefGoogle Scholar
  51. Tippery NP, Les DH (2011) Evidence for the hybrid origin of Nymphoides montana Aston (Menyanthaceae). Telopea 13:285–294CrossRefGoogle Scholar
  52. Wang QF, Guo YH, Haynes RR, Hellquist CB (2010) Hydrocharitaceae. In: Wu C-Y, Raven PH, Hong D-Y (eds) Flora of China, vol 23. Science Press. Beijing & Missouri Botanical Garden Press, St. Louis, pp 91–102Google Scholar
  53. Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants II. Kluwer Academic Publishing, Boston, pp 265–296CrossRefGoogle Scholar
  54. Wolf PG, Soltis PS, Soltis DE (1994) Phylogenetic relationships of Dennstaedtioid ferns: evidence from rbcL sequences. Mol Phylogenet Evol 3:383–392CrossRefGoogle Scholar
  55. Yang Z, Rannala B (1997) Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Mol Biol Evol 14:717–724CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Yu Ito
    • 1
    • 2
    Email author
  • Norio Tanaka
    • 3
  • Anders S. Barfod
    • 4
  • Josef Bogner
    • 5
  • Jie Li
    • 1
  • Okihito Yano
    • 6
  • Stephan W. Gale
    • 7
  1. 1.Plant Phylogenetics and Conservation Group, Centre for Integrative Conservation, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesKunmingPeople’s Republic of China
  2. 2.Faculty of Pharmaceutical SciencesSetsunan UniversityOsakaJapan
  3. 3.Tsukuba Botanical Garden, National Museum of Nature and ScienceTsukubaJapan
  4. 4.Department of BioscienceAarhus UniversityAarhus CDenmark
  5. 5.GersthofenGermany
  6. 6.Faculty of Biosphere-Geosphere ScienceOkayama University of ScienceOkayamaJapan
  7. 7.Kadoorie Farm and Botanic GardenHong KongPeople’s Republic of China

Personalised recommendations