Plant Systematics and Evolution

, Volume 302, Issue 8, pp 1027–1045 | Cite as

Morphometrics and molecular phylogenetics of Angraecum section Dolabrifolia (Orchidaceae, Angraecinae)

  • Murielle Simo-Droissart
  • Bonaventure Sonké
  • Vincent Droissart
  • Claire Micheneau
  • Porter P. LowryII.
  • Olivier J. Hardy
  • Gregory M. Plunkett
  • Tariq Stévart
Original Article

Abstract

Species delimitation within Angraecum section Dolabrifolia is problematic due to morphological variability coupled with overlap in many of the characters traditionally used to distinguish species. Recent molecular phylogenetic studies of the genus included three of the five currently described species of the Dolabrifolia group, placing them as sister to continental African species of Angraecum sect. Pectinaria. In preparation for a taxonomic revision of section Dolabrifolia, we analyzed morphological and molecular data to re-assess the circumscription of each of the five currently described species, examined the relationships among members of the section, and assessed their position within the genus. We used 172 alcohol-preserved specimens to perform multivariate analyses on 15 morphological characters. We also collected molecular sequence data from 16 taxa including all members of the section using six DNA regions, and analyzed these data with parsimony and Bayesian methods. The morphometric study revealed five distinct groups, of which four correspond to currently recognized species, while the fifth represents a taxonomic novelty. Angraecum podochiloides is the most distinctive morphologically, recognizable by its narrow leaves bearing white-yellowish flowers. The often confused species Angraecum distichum and Angraecum bancoense are clearly distinguishable by flower size. Molecular phylogenetic analyses indicated that section Dolabrifolia forms a well-supported clade related to the continental African members of section Pectinaria. Four species are well delimited, while the accessions of Angraecum aporoides formed two well-supported clades corresponding to two subclusters revealed by the morphometric study. The recently published Angraecum poppendickianum is shown to be a synonym of A. distichum.

Keywords

Angraecoid orchids Bayesian analyses Continental Africa Monophyly Morphometrics Parsimony 

Supplementary material

606_2016_1315_MOESM1_ESM.pdf (153 kb)
Online Resource 1. Material used for morphological study of species of Angraecum section Dolabrifolia
606_2016_1315_MOESM2_ESM.pdf (123 kb)
Online Resource 2. Species names with ID DNA, distribution and voucher information for all taxa used in this study
606_2016_1315_MOESM3_ESM.pdf (69 kb)
Online Resource 3. Alignment used to produce the tree with the ITS-1 marker
606_2016_1315_MOESM4_ESM.pdf (102 kb)
Online Resource 4. Alignment used to produce the tree with the rps16 marker
606_2016_1315_MOESM5_ESM.pdf (81 kb)
Online Resource 5. Alignment used to produce the tree with the trnL-F marker
606_2016_1315_MOESM6_ESM.pdf (117 kb)
Online Resource 6. Alignment used to produce the tree with the matK marker
606_2016_1315_MOESM7_ESM.pdf (116 kb)
Online Resource 7. Alignment used to produce the tree with the ycf1 marker
606_2016_1315_MOESM8_ESM.pdf (93 kb)
Online Resource 8. Alignment used to produce the tree with the trnC-petN marker
606_2016_1315_MOESM9_ESM.pdf (272 kb)
Online Resource 9. Alignment used to produce the tree with the five plastid markers
606_2016_1315_MOESM10_ESM.pdf (287 kb)
Online Resource 10. Alignment used to produce the tree with the six markers
606_2016_1315_MOESM11_ESM.pdf (96 kb)
Online Resource 11. Loadings of the first three axes of the extended principal component analysis on the 172 specimens of section Dolabrifolia, eigenvalues, percentage of variance, and cumulative percentage of variance explained by these first three axes. In bold, the highest loadings of each principal component. See Table 1 for variable codes

References

  1. Arends JC, van der Burg WJ, van der Laan FM (1980) Notes on African orchids. In: Arends JC, Boelema G, de Groot CT, Leewenberg AJM (eds) Miscellaneous papers Landbouwhogeschool 19. Wageningen, Veenman H & Zonen BV, pp 23–36Google Scholar
  2. Blattner FR (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR. Biotechniques 27:1180–1186PubMedGoogle Scholar
  3. Borg I, Groenen P (1997) Modern multidimensional scaling: theory and applications. Springer series in statistics. Springer, New YorkCrossRefGoogle Scholar
  4. Bory de Saint Vincent JBGM (1804) Voyage dans les quatre principales îles des mers d’Afrique. F. Buisson, ParisGoogle Scholar
  5. Cameron KM (2004) Utility of plastid psaB gene sequences for investigating intrafamilial relationships within Orchidaceae. Molec Phylogen Evol 31:1157–1180. doi:10.1016/j.ympev.2003.10.010 CrossRefGoogle Scholar
  6. Cameron KM, Chase MW (1999) Phylogenetic relationships of Pogoniinae (Vanilloideae, Orchidaceae): an herbaceous example of the eastern North America–eastern Asia phytogeographic disjunction. J Pl Res 112:317–329CrossRefGoogle Scholar
  7. Cameron KM, Chase MW, Whitten WM, Kores PJ, Jarrell DC, Albert VA, Yukawa T, Hills HG, Goldman DH (1999) A phylogenetic analysis of the Orchidaceae: evidence from rbcL nucleotide sequences. Amer J Bot 86:208–224CrossRefGoogle Scholar
  8. Carlsward BS, Whitten WM, Williams NH (2003) Molecular phylogenetics of Neotropical leafless Angraecinae (Orchidaceae): reevaluation of generic concepts. Int J Pl Sci 164:43–51. doi:10.1086/344757 CrossRefGoogle Scholar
  9. Carlsward BS, Stern WL, Bytebier B (2006a) Comparative vegetative anatomy and systematics of the angraecoids (Vandeae, Orchidaceae) with an emphasis on the leafless habit. Bot J Linn Soc 151:165–218. doi:10.1111/j.1095-8339.2006.00502.x CrossRefGoogle Scholar
  10. Carlsward BS, Whitten WM, Williams NH, Bytebier B (2006b) Molecular phylogenetics of Vandeae (Orchidaceae) and the evolution of leaflessness. Amer J Bot 93:770–786. doi:10.3732/ajb.93.5.770 CrossRefGoogle Scholar
  11. Chase MW, Hills HG (1991) Silica gel: an ideal desiccant for preserving field-collected leaves for use in molecular studies. Taxon 40:215–220. doi:10.2307/1222975 CrossRefGoogle Scholar
  12. Chase MW, Cameron KM, Hills HG, Jarrell D (1994) Molecular systematics of the Orchidaceae and other lilioid monocots. In: Pridgeon AM (ed) Proceedings of the 14th world orchid conference. Her Majesty’s Stationary Office, London, pp 61–73Google Scholar
  13. Chase MW, Cameron KM, Freudenstein JV, Pridgeon AM, Salazar G, Berg C, Schuiteman A (2015) An updated classification of Orchidaceae. Bot J Linn Soc 177:151–174CrossRefGoogle Scholar
  14. Chessel D, Dufour A-B, Thioulouse J (2004) The ade4 package. I. One-table methods. R News 4:5–10Google Scholar
  15. Cuenoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ, Chase MW (2002) Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. Amer J Bot 89:132–144CrossRefGoogle Scholar
  16. Cupido CN (2003) Systematic studies in the genus Merciera (Campanulaceae): a re-assessment of species boundaries. Adansonia 25:33–44Google Scholar
  17. Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Soft 22:1–20CrossRefGoogle Scholar
  18. Dray S, Dufour A-B, Chessel D (2007) The ade4 package II: two-table and K-table methods. R news 7:47–52Google Scholar
  19. Droissart V (2009) Étude taxonomique et biogéographique des plantes endémiques d’Afrique centrale atlantique: le cas des Orchidaceae. PhD thesis, Université Libre de BruxellesGoogle Scholar
  20. Droissart V, Sonké B, Stévart T (2006) Les Orchidaceae endémiques d’Afrique centrale atlantique présentes au Cameroun. Syst & Geogr Pl 76:3–84Google Scholar
  21. Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  22. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2005) Geneious Pro, version 6. Program distributed by Biomatters. Available at: http://www.geneious.com. Accessed 25 Oct 2015
  23. Efron B (1979) Bootstrap methods: another look at the jackknife. Ann Stats 7:1–26CrossRefGoogle Scholar
  24. Fay MF, Chase MW (2009) Orchid biology: from Linnaeus via Darwin to the 21st century. Ann Bot 104:359–364. doi:10.1093/aob/mcp190 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  26. Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416CrossRefGoogle Scholar
  27. Garay LA (1973) Systematics of the genus Angraecum (Orchidaceae). Kew Bull 28:495–516CrossRefGoogle Scholar
  28. Giraudoux P (2013) Pgirmess: data analysis in ecology. R package version 1.5.7. Available at: http://CRAN.R-project.org/package=pgirmess. Accessed 10 Mar 2015
  29. Goldman DH, Freudenstein JV, Kores PJ, Molvray M, Jarrell DC, Whitten WM, Cameron KM, Jansen RK, Chase MW (2001) Phylogenetics of Arethuseae (Orchidaceae) based on plastid matK and rbcL sequences. Syst Bot 26:670–695Google Scholar
  30. Górniak M, Paun O, Chase MW (2010) Phylogenetic relationships within Orchidaceae based on a low-copy nuclear coding gene, Xdh: congruence with organellar and nuclear ribosomal DNA results. Molec Phylogen Evol 56:784–795. doi:10.1016/j.ympev.2010.03.003 CrossRefGoogle Scholar
  31. Govaerts R, Bernet P, Kratochvil K, Gerlach G, Carr G, Alrich P, Pridgeon AM, Pfahl J, Campacci MA, Holland Baptista D, Tigges H, Shaw J, Cribb PJ, George A, Kreuz K, Wood J (2016) World Checklist of Orchidaceae The Board of Trustees of the Royal Botanic Gardens, Kew. Available at: http://www.kew.org/wcsp/. Accessed 20 Feb 2016
  32. Graves S, Piepho H-P, Selzer L, with help from Dorai-Raj S (2012) multcompView: visualizations of paired comparisons. Available at: http://CRAN.R-project.org/package=multcompView. Accessed 10 Oct 2015
  33. Hill MO, Smith AJE (1976) Principal component analysis of taxonomic data with multi-state discrete characters. Taxon 25:249–255CrossRefGoogle Scholar
  34. Hollander M, Wolfe DA (1973) Nonparametric statistical methods. Wiley, New YorkGoogle Scholar
  35. Huelsenbeck JP, Larget B, Alfaro ME (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molec Biol Evol 21:1123–1133. doi:10.1093/molbev/msh123 CrossRefPubMedGoogle Scholar
  36. Johnson LA, Soltis DE (1994) Matk DNA-sequences and phylogenetic reconstruction in Saxifragaceae S-Str. Syst Bot 19:143–156CrossRefGoogle Scholar
  37. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lee C, Wen J (2003) Phylogeny of Panax using chloroplast trnC-trnD intergenic region and the utility of trnC–trnD in interspecific studies of plants. Molec Phylogen Evol 31:894–903. doi:10.1016/j.ympev.2003.10.009 CrossRefGoogle Scholar
  39. Lindley J (1836) Edwards’s botanical register, vol 21. James Ridgway and sons, LondonGoogle Scholar
  40. Marcysiak K, Mazur M, Romo A, Montserrat JM, Didukh Y, Boratyńska K, Jasińska A, Kosiński P, Boratyński A (2007) Numerical taxonomy of Juniperus thurifera, J. excelsa and J. foetidissima (Cupressaceae) based on morphological characters. Bot J Linn Soc 155:483–495. doi:10.1111/j.1095-8339.2007.00730.x CrossRefGoogle Scholar
  41. Martos F, Johnson SD, Peter CI, Bytebier B (2014) A molecular phylogeny reveals paraphyly of the large genus Eulophia (Orchidaceae): a case for the reinstatement of Orthochilus. Taxon 63:9–23. doi:10.12705/631.6 CrossRefGoogle Scholar
  42. Mayr E (1969) The biological meaning of species. Biol J Linn Soc 1:311–320CrossRefGoogle Scholar
  43. Micheneau C, Carlsward BS, Fay MF, Bytebier B, Pailler T, Chase MW (2008) Phylogenetics and biogeography of Mascarene angraecoid orchids (Vandeae, Orchidaceae). Molec Phylogen Evol 46:908–922. doi:10.1016/j.ympev.2007.12.001 CrossRefGoogle Scholar
  44. Molvray MP, Kores J, Chase MW (2000) Polyphyly of mycoheterotrophic orchids and functional influences on floral and molecular characters. In: Wilson KL, Morrison DA (eds) Monocots: systematics and evolution. CSIRO Publishing, Collingwood, pp 441–448Google Scholar
  45. Mytnik-Ejsmont J, Szlachetko DL, Baranow P, Górniak M (2013) A phylogenetic and morphological study of Polystachya sect. Superpositae (Orchidaceae) with description of a new species from Cameroon. Pl Syst Evol. doi:10.1007/s00606-013-0856-0 Google Scholar
  46. Neubig KM, Whitten W, Carlsward BS, Blanco M, Endara L, Williams NH, Moore M (2009) Phylogenetic utility of ycf 1 in orchids: a plastid gene more variable than mat K. Pl Syst Evol 277:75–84. doi:10.1007/s00606-008-0105-0 CrossRefGoogle Scholar
  47. 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. doi:10.1093/bioinformatics/btm388 CrossRefPubMedGoogle Scholar
  48. Oxelman B, Liden M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Pl Syst Evol 206:393–410CrossRefGoogle Scholar
  49. Piepho H-P (2004) An algorithm for a letter-based representation of all-pairwise comparisons. J Comput Graph Stat 13:456–466. doi:10.1198/1061860043515 CrossRefGoogle Scholar
  50. Poulsen AD, Nordal I (2005) A phenetic analysis and revision of Guineo-Congolean rain forest taxa of Chlorophytum (Anthericaceae). Bot J Linn Soc 148:1–20. doi:10.1111/j.1095-8339.2005.00386.x CrossRefGoogle Scholar
  51. Pridgeon AM, Cribb PJ, Chase MW, Rasmussen FN (2014) Genera Orchidacearum, volume 6: Epidendroideae (Part 3). Oxford University Press, New YorkGoogle Scholar
  52. Purvis A, Gittleman JL, Brooks T (2005) Phylogeny and conservation. Cambridge University Press, New YorkCrossRefGoogle Scholar
  53. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at: http://www.R-project.org/. Accessed 10 Oct 2015
  54. Rakotoarivelo FP, Razafimandimbison SG, Mallet B, Faliniaina L, Pailler T (2012) Molecular systematics and evolutionary trends and relationships in the genus Jumellea (Orchidaceae): implications for its species limits. Taxon 61:534–544Google Scholar
  55. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. doi:10.1093/bioinformatics/btg180 CrossRefPubMedGoogle Scholar
  56. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Royston JP (1982) An extension of Shapiro and Wilk’s W test for normality to large samples. Appl Stat 31:115–124CrossRefGoogle Scholar
  58. Russell A, Samuel R, Rupp B, Barfuss MHJ, Safran M, Besendorfer V, Chase MW (2010) Phylogenetics and cytology of a pantropical orchid genus Polystachya (Polystachyinae, Vandeae, Orchidaceae): evidence from plastid DNA sequence data. Taxon 59:389–404Google Scholar
  59. Siegel S, Castellan NJ (1988) Non parametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill Humanities/Social Sciences/Languages, New YorkGoogle Scholar
  60. Simo TMM (2014) Étude taxonomique et phylogénétique de deux sections du genre Angraecum (Orchidaceae) en Afrique continentale et dans les îles du Golfe de Guinée. PhD thesis, University of Yaoundé I, CamerounGoogle Scholar
  61. Simo M, Sonké B, Droissart V, Stévart T (2010) Little-known Angraecums. The genus in Central Africa with a focus on two sections. Orchids 79:690–695Google Scholar
  62. Simo-Droissart M, Micheneau C, Sonké B, Droissart V, Lowry PP II, Plunkett GM, Hardy OJ, Stévart T (2013) Morphometrics and molecular phylogenetics of the continental African species of Angraecum section Pectinaria (Orchidaceae). Pl Ecol Evol 146:295–309. doi:10.5091/plecevo.2013.900 CrossRefGoogle Scholar
  63. Simo-Droissart M, Sonké B, Droissart V, Geerinck D, Micheneau C, Lowry PP II, Plunkett GM, Hardy OJ, Stévart T (2014) Taxonomic revision of the continental African species of Angraecum section Pectinaria (Orchidaceae). Syst Bot 39:725–739. doi:10.1600/036364414X682184 CrossRefGoogle Scholar
  64. Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. A series of books in biology. Freeman WH & Co, San FranciscoGoogle Scholar
  65. Stévart T (2003) Étude taxonomique, écologique et phytogéographique des Orchidaceae en Afrique centrale atlantique. PhD thesis, Université Libre de BruxellesGoogle Scholar
  66. Summerhayes VS (1966) African orchids: XXX. Kew Bull 20:165–199CrossRefGoogle Scholar
  67. Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (and other methods) version 4.0 b10. Sinauer Sunderland, MassachussetsGoogle Scholar
  68. Szlachetko DL, Olszewski TS (2001) Orchidacées 3. In: Achoundong G, Morat P (eds) Flore du Cameroun 36. MNHN, Paris, pp 666–948Google Scholar
  69. Szlachetko DL, Romowicz A (2007) Dolabrifolia, un nouveau genre d’orchidées de l’alliance Angraecum. Richardiana 7:53–54Google Scholar
  70. Szlachetko DL, Tukałło P, Mytnik-Ejsmont J, Grochocka E (2013) Reclassification of the Angraecum-alliance (Orchidaceae, Vandoideae) based on molecular and morphological data. Biodivers Res Conservation 29:1–23. doi:10.2478/biorc-2013-0004 CrossRefGoogle Scholar
  71. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109CrossRefGoogle Scholar
  72. The Plant List (2013) Version 1.1. Available at: http://www.theplantlist.org. Accessed 3 Mar 2016
  73. Thiers B (continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff New York Botanical Garden. Available at: http://sciweb.nybg.org/science2/IndexHerbariorum.asp. Accessed 25 Oct 2015
  74. van den Berg C, Higgins WE, Dressler RL, Whitten WM, Arenas S, Culham A, Chase MW (2000) A phylogenetic analysis of Laeliinae (Orchidaceae) based on sequence data from internal transcribed spacers (ITS) of nuclear ribosomal DNA. Lindleyana 15:96–114Google Scholar
  75. White F (1979) The Guineo-Congolian Region and its relationships to other phytochoria. Bull Jard Bot Natl Belg 49:11–55CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  • Murielle Simo-Droissart
    • 1
  • Bonaventure Sonké
    • 1
    • 2
    • 3
  • Vincent Droissart
    • 1
    • 2
    • 4
    • 5
  • Claire Micheneau
    • 6
  • Porter P. LowryII.
    • 2
    • 7
  • Olivier J. Hardy
    • 3
  • Gregory M. Plunkett
    • 8
  • Tariq Stévart
    • 2
    • 5
    • 9
  1. 1.Plant Systematics and Ecology Laboratory, Higher Teachers’ Training CollegeUniversity of Yaoundé IYaoundéCameroon
  2. 2.Missouri Botanical Garden, Africa and Madagascar DepartmentSt. LouisUSA
  3. 3.Evolutionary Biology and Ecology, Faculty of SciencesUniversité Libre de BruxellesBrusselsBelgium
  4. 4.Institut de Recherche pour le Développement (IRD), Unité Mixte de Recherche AMAP (Botanique et Bioinformatique de l’Architecture des Plantes)Montpellier CEDEX 5France
  5. 5.Herbarium et Bibliothèque de Botanique africaineUniversité Libre de BruxellesBrusselsBelgium
  6. 6.Université de La RéunionPeuplements Végétaux & Bioagresseurs Milieu Tropical, Unité Mixte de Recherche C53 Centre International de Recherche Agronomique pour le DéveloppementLa RéunionFrance
  7. 7.Institut de Systématique, Évolution, Biodiversité (ISYEB), Unité Mixte de Recherche 7205, Centre National de la Recherche Scientifique/Muséum National d’Histoire Naturelle/École Pratique des Hautes ÉtudesUniversité Pierre et Marie Curie, Sorbonne UniversitésParis CEDEX 5France
  8. 8.Cullman Program for Molecular SystematicsThe New York Botanical GardenBronxUSA
  9. 9.Agentschap Plantentuin MeiseDomein van BouchoutMeiseBelgium

Personalised recommendations