Plant Systematics and Evolution

, Volume 304, Issue 5, pp 699–721 | Cite as

New insights into variation, evolution and taxonomy of fairy lanterns (Thismia, Thismiaceae) with four new species from Borneo

  • Michal SochorEmail author
  • Michal Hroneš
  • Martin Dančák
Original Article


Fairy lanterns (Thismia Griff.) is a genus of poorly known mycoheterotrophic plants with unclear infrageneric classification. Commonly used approaches that utilize just a single or few traits in higher-level taxonomy lead to an apparently artificial system. In this contribution, four new species from Sarawak, northern Borneo, are described and illustrated. Thismia acuminata, T. laevis and T. nigra belong undoubtedly to section Sarcosiphon. Thismia viridistriata exhibits a high morphological variability with some individuals fitting section Scaphiophora based on the presence of a column on the top of the mitre, but otherwise perfectly matching the morphological characteristic of section Sarcosiphon. Five-locus (SSU, ITS, LSU, matR, atpA) phylogeny inference revealed paraphyly or polyphyly in the studied infrageneric taxa and showed that the importance of some traits traditionally used in Thismia taxonomy was overestimated. Most of the markers provide comparable phylogenetic signal; LSU performs best and is highly recommended for further phylogenetic studies. On the other hand, ITS is hypervariable and thus informative only within (sub)sections, as well as on intraspecific level, as proven in T. viridistriata with two distinct ITS (and also LSU and matR) alleles and two morphotypes within a small geographic area, which leads to an assumption of strong reproductive isolation even among nearby populations. For delimitation of species, the key trait appears to be the structure of the connective and any of the molecular markers used here.


Fairy lanterns Kelabit Highlands Mycoheterotrophy Pulong Tau Sarcosiphon Thismia 



We thank John Rian Pasan and David Attu for guiding services, Nur Afiza Binti Umar (Sarawak Forestry Department) for providing us with all the permits, Zuzana Egertová for field assistance and staff of SAR herbarium, particularly Nur Safinas Binti Jelani, for kind cooperation. We are also grateful to Renata Melichárková for line drawings. MH was supported by the project no. IGA PrF-2018-001 from the Internal Grant Agency of the Palacký University, and MS was supported by Grant No. LO1204 (Sustainable development of research in the Centre of the Region Haná) from the National Program of Sustainability I, MEYS. The research was conducted under the permit No. NCCD.907.4.4(JLD.13)-337 issued by Sarawak Forestry Department.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

606_2018_1504_MOESM1_ESM.pdf (465 kb)
Supplementary material 1 (PDF 464 kb)
606_2018_1504_MOESM2_ESM.pdf (19 kb)
Supplementary material 2 (PDF 19 kb)
606_2018_1504_MOESM3_ESM.pdf (726 kb)
Supplementary material 3 (PDF 725 kb)
606_2018_1504_MOESM4_ESM.txt (406 kb)
Supplementary material 4 (TXT 405 kb)


  1. Bidartondo MI (2005) The evolutionary ecology of myco-heterotrophy. New Phytol 167:335–352. CrossRefPubMedGoogle Scholar
  2. Blume CL (1850) Burmanniaceae. Mus Bot Lugduno-Batavum 1(5):65–80Google Scholar
  3. Chantanaorrapint S, Suddee S (2018) Thismia thaithongiana (Dioscoreaceae: Thismieae), a new species of mycoheterotroph from an unusual habitat. Phytotaxa 333:287–292. CrossRefGoogle Scholar
  4. Chantanaorrapint S, Tetsana N, Sridith K (2015) Notes on Thismia clandestina (Thismiaceae), a little-known mycoheterotrophic species. Polish Bot J 60:71–74. Google Scholar
  5. Chantanaorrapint S, Wai JS, Poopath M, Tetsana N (2016) Thismia claviformis (Thismiaceae), a new species from the Thai-Malay Peninsula. Phytotaxa 280:292–296. CrossRefGoogle Scholar
  6. Chiang P-Y, Hsieh T-H (2011) Thismia huangii (Thismiaceae), a new species from Taiwan. Taiwania 56:138–142Google Scholar
  7. Cooper WE (2017) Thismia hawkesii W.E.Cooper and T. lanternatus W.E.Cooper (Thismiaceae), two new fairy lantern species from the Wet Tropics Bioregion, Queensland, Australia. Austrobaileya 10:130–138Google Scholar
  8. Dančák M, Hroneš M, Sochor M, Kobrlová L, Hédl R, Hrázský Z, Vildomcová A, Sukri RS, Metali F (2013) A new species of Thismia (Thismiaceae) from Brunei Darussalam, Borneo. Phytotaxa 125:33–39. CrossRefGoogle Scholar
  9. Darriba D, Taboada GL, Doallo RR, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772. CrossRefGoogle Scholar
  10. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  11. Eyre-Walker A, Gaut BS (1997) Correlated rates of synonymous site evolution across plant genomes. Molec Biol Evol 14:455–460. CrossRefPubMedGoogle Scholar
  12. Govaerts R, Wilkin P, Saunders RM (2007) World checklist of Dioscoreales: yams and their allies. Royal Botanic Gardens, KewGoogle Scholar
  13. Hroneš M (2016) Genus Thismia Griff. (Thismiaceae) in Asia and Australasia with focus on the Malesian floristic region. Palacky University, OlomoucGoogle Scholar
  14. Hroneš M, Kobrlová L, Taraška V, Popelka O, Hédl R, Sukri RS, Metali F, Dančák M (2015) Thismia brunneomitra, another new species of Thismia (Thismiaceae) from Ulu Temburong, Brunei Darussalam. Phytotaxa 234:172–178. CrossRefGoogle Scholar
  15. Hroneš M, Rejžek M, Sochor M, Svátek M, Kvasnica J, Egertová Z, Pereira JT, Nilus R, Dančák M (2018) Two new species of Thismia subsect. Odoardoa (Thismiaceae) from Borneo. Pl Ecol Evol (in press).
  16. Hunt CA, Steenbeeke G, Merckx VSFT (2014) Thismia megalongensis (Thismiaceae), a new species of Thismia from New South Wales. Telopea 16:165–174. Google Scholar
  17. Imhof S, Massicotte HB, Melville LH, Peterson RL (2013) Subterranean morphology and mycorrhizal structures. In: Merckx VSFT (ed) Mycoheterotrophy. Springer, New York, pp 157–214CrossRefGoogle Scholar
  18. IUCN (2012) and Criteria: version 3.1, 2nd edn. IUCN, Gland. Available at:
  19. Jarvie JK (1996) Thismia lauriana (Burmanniaceae), a new species from Central Kalimantan. Blumea 41:57–259Google Scholar
  20. Jonker FP (1938) A monograph of the Burmanniaceae. Meded Bot Mus Herb Rijks Univ Utrecht 51:1–279Google Scholar
  21. Jonker FP (1948) Burmanniaceae. In: van Steenis CGGJ (ed) Flora Malesiana I, 4. Noordhoff-Kolf, Leiden, pp 13–26Google Scholar
  22. Kay KM, Sargent RD (2009) The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annual Rev Ecol Evol Syst 40:637–656. CrossRefGoogle Scholar
  23. Kiew R (1999) Thismia goodii (Burmanniaceae), the Blue-capped Thismia, a new species from Borneo. Gard Bull Singapore 51:179–182Google Scholar
  24. Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyasek R, Rocca J, Soltis DE, Soltis PS (2005) Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics 169:931–944. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kumar P, Gale SW, Li J, Bouamanivong S, Fischer GA (2017) Thismia nigricoronata, a new species of Burmanniaceae (Thismieae, Dioscoreales) from Vang Vieng, Vientiane Province, Laos, and a key to subgeneric classification. Phytotaxa 319:225–240. CrossRefGoogle Scholar
  26. Kuzoff RK, Sweere JA, Soltis DE, Soltis PS, Zimmer EA (1998) The phylogenetic potential of entire 26S rDNA sequences in plants. Molec Biol Evol 15:251–263. CrossRefPubMedGoogle Scholar
  27. Lanfear R, Frandsen PB, Wright AM et al (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molec Biol Evol 34:772–773. PubMedGoogle Scholar
  28. Maas PJM, Maas-van de Kamer H, van Benthem J, Snelders HCM, Rübsamen T (1986) Burmanniaceae. Fl Neotrop Monogr 42:1–189Google Scholar
  29. Mar SS, Saunders R (2015) Thismia hongkongensis (Thismiaceae): a new mycoheterotrophic species from Hong Kong, China, with observations on floral visitors and seed dispersal. PhytoKeys 46:21–33. CrossRefGoogle Scholar
  30. Meng S-W, Chen Z-D, Li D-Z, Liang H-X (2002) Phylogeny of Saururaceae based on mitochondrial matR gene sequence data. J Pl Res 115:71–76. CrossRefGoogle Scholar
  31. Merckx VSFT, Schols P, Maas-van de Kamer H, Maas P, Huysmans S, Smets E (2006) Phylogeny and evolution of Burmanniaceae (Dioscoreales) based on nuclear and mitochondrial data. Amer J Bot 93:1684–1698CrossRefGoogle Scholar
  32. Merckx VSFT, Janssens SB, Hynson NA et al (2012) Mycoheterotrophic interactions are not limited to a narrow phylogenetic range of arbuscular mycorrhizal fungi. Molec Ecol 21:1524–1532. CrossRefGoogle Scholar
  33. Merckx VSFT, Freudenstein JV, Kissling J, Christenhusz MJM, Stotler RE, Crandall-Stotler B, Wickett N, Rudall PJ, Maas-van de Kamer H, Maas PJM (2013a) Taxonomy and classification. In: Merckx VSFT (ed) Mycoheterotrophy. Springer, New York, pp 19–101CrossRefGoogle Scholar
  34. Merckx VSFT, Smets EF, Specht CD (2013b) Biogeography and conservation. In: Merckx VSFT (ed) Mycoheterotrophy. Springer, New York, pp 103–156CrossRefGoogle Scholar
  35. Merckx VSFT, Gomes SIF, Wapstra M, Hunt C, Steenbeeke G, Mennes CB, Walsh N, Smissen R, Hsieh TH, Smets Bidartondo MI (2017) The biogeographical history of the interaction between mycoheterotrophic Thismia (Thismiaceae) plants and mycorrhizal Rhizophagus (Glomeraceae) fungi. J Biogeogr 44:1869–1879. CrossRefGoogle Scholar
  36. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna 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. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Schlechter FRR (1921) Die Thismieae. Notizbl Königl Bot Gart Berlin 8:31–45Google Scholar
  38. Smith JJ (1911) Beiträge zur Kenntnis der Saprophyten Javas. IV. Zur Systematik von Thismia clandestina Miq. und Thismia Versteegii J. J. Smith. Ann Jard Bot Buitenzorg 24:55–59Google Scholar
  39. Sochor M, Vašut RJ, Sharbel TF, Trávníček B (2015) How just a few makes a lot: speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Molec Phylogen Evol 89:13–27. CrossRefGoogle Scholar
  40. Sochor M, Sukri RS, Metali F, Dančák M (2017) Thismia inconspicua (Thismiaceae), a new mycoheterotrophic species from Borneo. Phytotaxa 295:263–270. CrossRefGoogle Scholar
  41. Suetsugu K, Tsukaya H, Tagane S, Suddee S, Rueangruea S, Yahara T (2017) Thismia brunneomitroides (Thismiaceae), a new mycoheterotrophic species from southern Thailand. Phytotaxa 314:103–109. CrossRefGoogle Scholar
  42. Suetsugu K, Tsukaya H, Tagane S et al (2018) Flora of Bokor National Park VII: Thismia bokorensis (Burmanniaceae), a new species representing a new generic record. Phytotaxa 334:65–69. CrossRefGoogle Scholar
  43. Sujanapal P, Robi AJ, Dantas KJ, Sumod M, Merckx VSFT (2017) Thismia (Thismiaceae): the first record of the mycoheterotrophic genus to the Flora of India with a new species revealing the phytogeographical significance of Western Ghats. Blumea 62:97–102. CrossRefGoogle Scholar
  44. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molec Biol Evol 28:2731–2739. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tsukaya H, Okada H (2012) A new species of Thismia (Thismiaceae) from West Kalimantan, Borneo. Syst Bot 37:53–57. CrossRefGoogle Scholar
  46. Tsukaya H, Suleiman M, Okada H (2014) A new variety of Thismia hexagona Dančák, Hroneš, Koblová et Sochor (Thismiaceae) from Sabah, Borneo, Malaysia. Acta Phytotaxon Geobot 65:141–145Google Scholar
  47. Tsukaya H, Suetsugu K, Suleiman M (2017) Thismia bryndonii (Thismiaceae), a new species from Maliau Basin, Sabah, Borneo. Phytotaxa 312:135–138. CrossRefGoogle Scholar
  48. White TJ, Bruns T, Lee S, Taylor JW (1990) 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 315–322Google Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre of the Region Haná for Biotechnological and Agricultural Research, Department of Genetic Resources for Vegetables, Medicinal and Special PlantsCrop Research InstituteOlomoucCzech Republic
  2. 2.Department of BotanyPalacký UniversityOlomoucCzech Republic
  3. 3.Department of Ecology and Environmental SciencesPalacký UniversityOlomoucCzech Republic

Personalised recommendations