Abstract
Recent molecular studies have suggested the monophyly of Bolusiella, a small orchid genus comprising five species and one subspecies from Continental Africa, but sampling has been limited. Using the species delimitation presented in the recent taxonomic revision of the genus, this study aimed to confirm the monophyly of Bolusiella and assess the interspecific relationships using a comprehensive sampling and various analytical methods. DNA sequences of one nuclear spacer region (ITS-1) and five plastid regions (matK, rps16, trnL–trnF, trnC–petN, and ycf1) from 20 specimens representing all five species of the genus were analyzed using static homology, dynamic homology, and Bayesian methods. The monophyly of both the genus Bolusiella and each of its five species was confirmed, corroborating the previously published taxonomic revision. The use of dynamic homology methods was not conclusive for this particular group. The results of the total evidence analysis (combining all six sequence regions) using the dynamic homology approach yielded a slightly different hypothesis regarding interspecific relationships (namely the exchange of B. talbotii and Bolusiella iridifolia as the earliest diverging lineage), probably because the nodes in question are supported by a small subset of conflicting characters, compared to the hypotheses resulting from the static homology and Bayesian methods, which are congruent with the results of previous studies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aagesen L (2005) Direct optimization, affine gap costs, and node stability. Molec Phylogen Evol 36:641–653. https://doi.org/10.1016/j.ympev.2005.04.012
Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Molec Phylogen Evol 29:417–434. https://doi.org/10.1016/S1055-7903(03)00208-2
Arango CP, Wheeler WC (2007) Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23:255–293. https://doi.org/10.1111/j.1096-0031.2007.00143.x
Barriel V, Tassy P (1998) Rooting with multiple outgroups: consensus versus parsimony. Cladistics 14:193–200. https://doi.org/10.1111/j.1096-0031.1998.tb00332.x
Blattner FR (1999) Direct amplification of the entire ITS region from poorly preserved plant material using recombinant PCR. Biotechniques 27:1180–1186
Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803. https://doi.org/10.1111/j.1558-5646.1988.tb02497.x
Carlsward BS, Stern W, 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. https://doi.org/10.1111/j.1095-8339.2006.00502.x
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. https://doi.org/10.3732/ajb.93.5.770
Catalano SA, Saidman BO, Vilardi JC (2009) Evolution of small inversions in chloroplast genome: a case study from a recurrent inversion in angiosperms. Cladistics 25:93–104. https://doi.org/10.1111/j.1096-0031.2008.00236.x
Chase MW, Hills HG (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220. https://doi.org/10.2307/1222975
Cialdella AM, Giussani LM, Aagesen L, Zuloaga FO, Morrone O (2007) A phylogeny of Piptochaetium (Poaceae: Pooideae: Stipeae) and related genera based on a combined analysis including trnL-F, rpl16, and morphology. Syst Bot 32:545–559. https://doi.org/10.1600/036364407782250607
Cialdella AM, Salariato DL, Aagesen L, Giussani LM, Zuloaga FO, Morrone O (2010) Phylogeny of new world stipeae (Poaceae): an evaluation of the monophyly of Aciachne and Amelichloa. Cladistics 26:563–578. https://doi.org/10.1111/j.1096-0031.2010.00310.x
Cuénoud 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 89:132–144. https://doi.org/10.3732/ajb.89.1.132
CodonCode Aligner (version 4.2.7) CodonCode Corporation. Available at: http://www.codoncode.com
Darlu P, Tassy P (1993) La reconstruction phylogénétique. Masson, Paris
D’Haese CA (2002) Were the first springtails semi-aquatic? A phylogenetic approach by means of 28S rDNA and optimization alignment. Proc Roy Soc London, Ser B, Biol Sci 269:1143. https://doi.org/10.1098/rspb.2002.1981
D’Haese CA (2003) Morphological appraisal of Collembola phylogeny with special emphasis on Poduromorpha and a test of the aquatic origin hypothesis. Zool Scripta 32:563–586. https://doi.org/10.1046/j.1463-6409.2003.00134.x
D’Haese CA (2004) Les principes de l’Optimisation Directe. Biosystema 22:49–58
Donoghue MJ, Olmstead RG, Smith JF, Palmer JD (1992) Phylogenetic relationships of dipsacales based on rbcL sequences. Ann Missouri Bot Gard 79:333–345. https://doi.org/10.2307/2399772
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19:11–15
Efron B (1979) Bootstrap methods: another look at the jackknife. Ann Stat 29:1–26
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Frost DR, Rodrigues MT, Grant T, Titus TA (2001) Phylogenetics of the lizard genus Tropidurus (Squamata: Tropiduridae: Tropidurinae): direct optimization, descriptive efficiency, and sensitivity analysis of congruence between molecular data and morphology. Molec Phylogen Evol 21:352–371. https://doi.org/10.1006/mpev.2001.1015
Giannini N (2003) A phylogeny of megachiropteran bats (Mammalia: Chiroptera: Pteropodidae) based on direct optimization analysis of one nuclear and four mitochondrial genes. Cladistics 19:496–511. https://doi.org/10.1016/j.cladistics.2003.09.002
Giribet G, Wheeler W (1999) On gaps. Molec Phylogen Evol 13:132–143. https://doi.org/10.1006/mpev.1999.0643
Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161. https://doi.org/10.1038/35093097
Gladstein D, Wheeler WC (1996) POY: phylogeny reconstruction via direct optimization. American Museum of Natural History, New York
Goloboff PA (1999) Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15:415–428. https://doi.org/10.1111/j.1096-0031.1999.tb00278.x
Gottlieb AM, Giberti GC, Poggio L (2005) Molecular analyses of the genus Ilex (Aquifoliaceae) in southern South America, evidence from AFLP and ITS sequence data. Amer J Bot 92:352–369. https://doi.org/10.3732/ajb.92.2.352
Geneious (version 4.8.5) Biomatters. Available at: http://www.geneious.com/
Heath Ogden T, Rosenberg MS (2006) How should gaps be treated in parsimony? A comparison of approaches using simulation. Molec Phylogen Evol 42:817–826. https://doi.org/10.1016/j.ympev.2006.07.021
Huelsenbeck JP, Larget B, Alfaro ME (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molec Biol Evol 21:1123–1133. https://doi.org/10.1093/molbev/msh123
Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19:143–156. https://doi.org/10.2307/2419718
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
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. https://doi.org/10.1016/j.ympev.2003.10.009
Lehtonen S, Myllys L (2008) Cladistic analysis of Echinodorus (Alismataceae): simultaneous analysis of molecular and morphological data. Cladistics 24:218–239. https://doi.org/10.1111/j.1096-0031.2007.00177.x
Mickevich MF, Farris JS (1981) The implications of congruence in Menidia. Syst Zool 30:351–370. https://doi.org/10.2307/2413255
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 441–448
Neubig KM, Whitten WM, Carlsward BS, Blanco MA, Endara L, Williams NH, Moore M (2009) Phylogenetic utility of ycf1 in orchids: a plastid gene more variable than matK. Pl Syst Evol 277:75–84. https://doi.org/10.1007/s00606-008-0105-0
Nixon KC (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414. https://doi.org/10.1111/j.1096-0031.1999.tb00277.x
Oxelman B, Lidén M, Berglund D (1997) Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Pl Syst Evol 206:393–410. https://doi.org/10.1007/BF00987959
Padial JM, Grant T, Frost DR (2014) Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria. Zootaxa 3825:1–132. https://doi.org/10.11646/zootaxa.3825.1.1
Pedraza-Peñalosa P (2010) Insensitive blueberries: a total evidence analysis of Disterigma s.l. (Ericaceae) exploring transformation costs. Cladistics 26:388–407. https://doi.org/10.1111/j.1096-0031.2009.00293.x
Petersen G, Aagesen L, Seberg O, Larsen IH (2011) When is enough, enough in phylogenetics? A case in point from Hordeum (Poaceae). Cladistics 27:428–446. https://doi.org/10.1111/j.1096-0031.2011.00347.x
Ronquist F, Huelsenbeck JP (2003) MrBayes: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1972–1974. https://doi.org/10.1093/bioinformatics/btg180
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. https://doi.org/10.1093/sysbio/sys029
Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381. https://doi.org/10.1080/10635159950173889
Simo-Droissart M, Micheneau C, Sonké B, Droissart V, Plunkett GM, Lowry P, Hardy OJ, Stévart T (2013) Morphometrics and molecular phylogenetics of the continental African species of Angraecum section Pectinaria (Orchidaceae). Pl Syst Evol 146:295–309. https://doi.org/10.5091/plecevo.2013.900
Simo-Droissart M, Sonké B, Droissart V, Micheneau C, Lowry P, Hardy OJ, Plunkett GM, Stévart T (2016) Morphometrics and molecular phylogenetics of Angraecum section Dolabrifolia (Orchidaceae, Angraecinae). Pl Syst Evol 302:1027–1045. https://doi.org/10.1007/s00606-016-1315-5
Souto DF, Catalano SA, Tosto D, Bernasconi P, Sala A, Wagner M, Corach D (2006) Phylogenetic relationships of Deschampsia antarctica (Poaceae): insights from nuclear ribosomal ITS. Pl Syst Evol 261:1–9. https://doi.org/10.1007/s00606-006-0425-x
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
Varon A, Vinh LS, Wheeler WC (2010) POY version 4: phylogenetic analysis using dynamic homologies. Cladistics 26:72–85. https://doi.org/10.1111/j.1096-0031.2009.00282.x
Verlynde S, Dubuisson JY, Stévart T, Simo M, Geerinck D, Sonké B, Cawoy V, Descourvières P, Droissart V (2013) Taxonomic revision of the genus Bolusiella (Orchidaceae, Angraecinae) with a new species from Cameroon, Burundi and Rwanda. Phytotaxa 114:1–22. https://doi.org/10.11646/phytotaxa.114.1.1
Weese TL, Johnson LA (2005) Utility of NADP-dependent isocitrate dehydrogenase for species-level evolutionary inference in angiosperm phylogeny: a case study in Saltugilia. Molec Phylogen Evol 36:24–41. https://doi.org/10.1016/j.ympev.2005.03.004
Wheeler WC (1996) Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12:1–9. https://doi.org/10.1111/j.1096-0031.1996.tb00189.x
Wheeler WC (2003) Iterative pass optimization of sequence data. Cladistics 19:254–260. https://doi.org/10.1111/j.1096-0031.2003.tb00368.x
Wheeler WC, Aagensen L, Arango CP, Faivovich J, Grant T, D’Haese CA, Janies D, Smith WL, Varon A, Giribet G (2006) Dynamic homology and phylogenetic systematics: a unified approach using POY. American Museum of Natural History, New York
Wheeler WC, Lucaroni N, Hong L, Crowley LM, Varón A (2014) POY version 5: phylogenetic analysis using dynamic homologies under multiple optimality criteria. Cladistics 31:189–196. https://doi.org/10.1111/cla.12083
Worsaae K, Nygren A, Rouse GW, Giribet G, Persson J, Sundberg P, Pleijel F (2005) Phylogenetic position of Nerillidae and Aberranta (Polychaeta, Annelida), analysed by direct optimization of combined molecular and morphological data. Zool Scripta 34:313–328. https://doi.org/10.1111/j.1463-6409.2005.00190.x
Acknowledgements
We want to thank Clément Schneider and Julio Pedraza for their assistance in the use of the Museum National d’Histoire Naturelle’s parallel mainframe cluster (PCIA, UMS2700) in the early stages of this project. The authors are grateful to the people growing orchids in the Yaoundé shadehouse (Cameroon), in the Sibang shadehouse (Gabon) and in the Nimba shadehouse (Republic of Guinea) for the collection of specimens and leaf samples. We would also like to thank Gilbert Delepierre, Jean-Paul Lebel, and Eberhard Fischer for the collection of leaf samples in Rwanda and Kenya. We are grateful to the American Orchid Society for financial support to M. Simo-Droissart, V. Droissart and T. Stévart. This research was supported by the US National Science Foundation (1051547, T. Stévart as PI, G. Plunkett as co-PI).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors of this paper “Molecular phylogeny of the genus Bolusiella (Orchidaceae, Angraecinae)” declare that they have no conflict of interest.
Additional information
Handling editor: Mark Mort.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Online Resource 1
Morphological differences among Bolusiella species: Diagnostic characters (in bold) distinguishing the six recognized species of Bolusiella. (PDF 77 kb)
Online Resource 2
Taxonomic sample for the molecular study: Missing data for concerned regions are indicated with “–” and available data with “+.” (PDF 78 kb)
Online Resource 3
Nucleotide sequence alignment matrix of 6 combined marker dataset (ITS-1, matK, rps16, trnL–F, trnC–petN and ycf1). (NEX 159 kb)
Online Resource 4
Additional phylogenetic trees resulting of each 5 chloroplast marker and the 5 chloroplast combined dataset obtained with Dynamic Homology analysis, Static Homology analysis (Maximum parsimony), with indels treated as characters, Static Homology analysis (Maximum parsimony), with indels treated as missing data and Bayesian analysis. (PDF 406 kb)
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Morphological differences among Bolusiella species: Diagnostic characters (in bold) distinguishing the six recognized species of Bolusiella.
Online Resource 2. Taxonomic sample for the molecular study: Missing data for concerned regions are indicated with “–” and available data with “+.”
Online Resource 3. Nucleotide sequence alignment matrix of 6 combined marker dataset (ITS-1, matK, rps16, trnL–F, trnC–petN and ycf1).
Online Resource 4. Additional phylogenetic trees resulting of each 5 chloroplast marker and the 5 chloroplast combined dataset obtained with Dynamic Homology analysis, Static Homology analysis (Maximum parsimony), with indels treated as characters, Static Homology analysis (Maximum parsimony), with indels treated as missing data and Bayesian analysis.
Rights and permissions
About this article
Cite this article
Verlynde, S., D’Haese, C.A., Plunkett, G.M. et al. Molecular phylogeny of the genus Bolusiella (Orchidaceae, Angraecinae). Plant Syst Evol 304, 269–279 (2018). https://doi.org/10.1007/s00606-017-1474-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-017-1474-z