Phylogeny of the Asian Hedyotis-Oldenlandia complex (Spermacoceae, Rubiaceae): Evidence for high levels of polyphyly and the parallel evolution of diplophragmous capsules

Molecular Phylogenetics and Evolution

Volumn 67, Issue 1, 2013, Pages 110-122

  Guo, Xing ^a   Wang, Rui Jiang ^a   Simmons, Mark P ^b   But, Paul Pui Hay ^c   Yu, Jing ^c  

^a SOUTH CHINA INSTITUTE OF BOTANY   (China)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Dimetia; Hedyotis Oldenlandia complex; Phylogeny; Rubiaceae; Scleromitrion; Thecagonum

Indexed keywords

HEDYOTIS; OLDENLANDIA; OLDENLANDIA CORYMBOSA; RUBIACEAE; SPERMACOCEAE;

EID: 84873461215     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.01.006     Document Type: Article

References (111)

1. Akaike H. A new look at the statistical model identification. IEEE Trans. Automat. Control. 1974, 19:716-723.
2. Álvarez I., Wendel J.F. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 2003, 29:417-434.
3. Andersson L., Rova J.H.E. The rps16 Intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Syst. Evol. 1999, 214:161-186.
4. Andersson L., Rova J.H.E., Guarin F.A. Relationships, circumscription, and biogeography of Arcytophyllum (Rubiaceae) based on evidence from cpDNA. Brittonia 2002, 54:40-49.
5. Babu C.R. Thecagonum Babu - a new generic name in Rubiaceae. Bull. Bot. Surv. India 1969, 11:213-214.
6. Bailey C.D., Carr T.G., Harris S.A., Hughes C.E. Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol. Phylogenet. Evol. 2003, 29:435-455.
7. Bakhuizen van den Brink R.C. Hedyotis L. Fl. Java (Spermatoph.) 1965, vol. 2:284-288. N.V.P. Noordhoff, Groningen.
8. Barrett S.C.H., Shore J.S. New insights on heterostyly: comparative biology, ecology and genetics. Self-Incompatibility in Flowering Plants - Evolution, Diversity, and Mechanisms 2008, 3-32. Springer-Verlag, Berlin. V.E. Franklin-Tong (Ed.).
9. Bentham, G., Hooker, J.D. 1873. Rubiaceae. Genera Plantarum, vol. 2, no. 1-2. Lovell Reeve & Co., London, pp. 7-151.
10. Bremekamp C.E.B. The African species of Oldenlandia L. sensu Hiern & K. Schumann. Verh. Kon. Ned. Akad. Wetensch. Afd. Natuurk. 1952, 48:1-197.
11. Bremer B. Phylogenetic studies within the Rubiaceae and relationships to other families based on molecular data. Opera Bot. Belg. 1996, 7:33-50.
12. Bremer B., Manen J.-F. Phylogeny and classification of the subfamily Rubioideae (Rubiaceae). Plant Syst. Evol. 2000, 225:43-72.
13. Bull J.J., Huelsenbeck J.P., Cunningham C.W., Swofford D.L., Waddell P.J. Partitioning and combining data in phylogenetic analysis. Syst. Biol. 1993, 42:384-397.
14. Castoe T.A., Doan T.M., Parkinson C.L. Data partitions and complex models in Bayesian analysis: the phylogeny of the gymnophthalmid lizards. Syst. Biol. 2004, 53:448-469.
15. Chen, T., Taylor, C.M., 2011. Hedyotis L. In: Wu, Z.Y., Raven, P. (Eds.), Fl. China. vol. 19. Science Press, Beijing & Missouri Botanical Garden Press, St. Louis, pp. 147-174.
16. Church S.A. Molecular phylogenetics of Houstonia (Rubiaceae): descending aneuploidy and breeding system evolution in the radiation of the lineage across North America. Mol. Phylogenet. Evol. 2003, 27:223-238.
17. Cuenoud P., Savolainen V., Chatrou L.W., Powell M., Grayer R., Chase M.W. Molecular phylogenetics of the Caryophyllales based on 18SrDNA, rbcL, atpB and matK sequences. Am. J. Bot. 2002, 89:132-144.
18. Davis J.I., Simmons M.P., Stevenson D.W., Wendel J.F. Data decisiveness, data quality, and incongruence in phylogenetic analysis: an example from the monocotyledons using mitochondrial atpA sequences. Syst. Biol. 1998, 47:282-310.
19. Davis J.I., Nixon K.C., Little D.P. The limits of conventional cladistic analysis. Parsimony, Phylogeny, and Genomics 2005, 119-147. Oxford University Press, Oxford. V.A. Albert (Ed.).
20. Dessein, S., 1998. Fylogenie van de Hedyotideae (Rubiaceae)-Een morfologische en anatomische studie van de Afrikaanse taxa. Master's Thesis, Katholieke Universiteit Leuven, Leuven, Belgium.
21. Dowrick V.P.J. Heterostyly and homostyly in Primula obconica. Heredity 1956, 10:219-236.
22. Doyle J.J. Gene trees and species trees: molecular systematics as one-character taxonomy. Syst. Bot. 1992, 17:144-163.
23. Doyle J.J. The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Syst. Bot. 1995, 20:574-588.
24. Dutta, R., Deb, D.B., 2004. Taxonomic revision of Hedyotis L. (Rubiaceae) in Indian subcontinent. Botanical Survey of India, Kolkata, pp. 1-211.
25. Farris J.S. The retention index and the rescaled consistency index. Cladistics 1989, 5:417-419.
26. Farris J.S., Albert V.A., Källersjö M., Lipscomb D., Kluge A.G. Parsimony jackknifing outperforms neighbor-joining. Cladistics 1996, 12:99-124.
27. Fay M.F., Swensen S.M., Chase M.W. Taxonomic affinities of Medusagyne oppositifolia (Medusagynaceae). Kew. Bull. 1997, 52:111-120.
28. Felsenstein J. Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Syst. Zool. 1973, 22:240-249.
29. Felsenstein J. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 1978, 27:401-410.
30. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783-791.
31. Fosberg F.R. The Polynesian species of Hedyotis (Rubiaceae). Bern. P. Bish. Mus. Bull. 1943, 174:3-102.
32. Fosberg F.R., Sachet M.-H. Studies in Indo-Pacific Rubiaceae. Allertonia 1991, 6:191-278.
33. Gaut B.S., Lewis P.O. Success of maximum likelihood phylogeny inference in the four-taxon case. Mol. Biol. Evol. 1995, 12:152-162.
34. Graham A. Fossil record of the Rubiaceae. Ann. Missouri Bot. Gard. 2009, 96:90-108.
35. Groeninckx I., Dessein S., Ochoterena H., Persson C., Motley T.J., Kårehed J., Bremer B., Huysmans S., Smets E. Phylogeny of the herbaceous tribe Spermacoceae (Rubiaceae) based on plastid DNA data. Ann. Missouri Bot. Gard. 2009, 96:109-132.
36. Groeninckx I., Block P.De., Robbrecht E., Smets E.E., Dessein S. Amphistemon and Thamnoldenlandia, two new genera of Rubiaceae (Spermacoceae) endemic to Madagascar. Bot. J. Linn. Soc. 2010, 163:447-472.
37. Groeninckx I., Ochoterena H., Smets E., Dessein S. Molecular phylogenetic and morphological study of Kohautia (Spermacoceae, Rubiaceae), with the recognition of the new genus Cordylostigma. Taxon 2010, 59:1457-1471.
38. Guo X., Wang R.J. Hedyotis xinyiensis (Rubiaceae), a new species from China. Ann. Bot. Fennici 2011, 48:443-447.
39. Guo X., Simmons M.P., But P.P.-H., Shaw P.C., Wang R.J. Application of DNA barcodes in Hedyotis L. (Spermacoceae, Rubiaceae). J. Syst. Evol. 2011, 49:203-212.
40. Halford D.A. Review of the genus Oldenlandia L. (Rubiaceae) and related genera in Australia. Austrobaileya 1992, 3:683-722.
41. Hudson R.R. Gene genealogies and the coalescent process. Oxf. Surv. Evol. Biol. 1990, 7:1-44.
42. Jarvis C.E. Seventy-two proposals for the conservation of types of selected Linnaean generic names, the report of Subcommittee 3C on the lectotypification of Linnaean generic names. Taxon 1992, 41:552-583.
43. Jovet P. Aux confins des Rubiacées et des Loganiacées. Notul. Syst. (Paris) 1941, 10:39-56.
44. Kårehed J., Groeninckx I., Dessein S., Motley T.J., Bremer B. The phylogenetic utility of chloroplast and nuclear DNA markers and the phylogeny of the Rubiaceae tribe Spermacoceae. Mol. Phylogenet. Evol. 2008, 49:843-866.
45. Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 2008, 9:286-298.
46. Katoh K., Toh H. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 2008, 9:212.
47. Kluge A.G. A concern for evidence and a phylogenetic hypothesis for relationships among Epicrates (Boidae, Serpentes). Syst. Zool. 1989, 38:7-25.
48. Kluge A.G., Farris J.S. Quantitative phyletics and the evolution of Anurans. Syst. Zool. 1969, 18:1-32.
49. Ko, W.C., 1999. Hedyotis L. In: Lo, H.S. (Ed.), Fl. Reipubl. Pop. Sin., vol. 71, no. 1. Science Press, Beijing, pp. 32-77.
50. Lamarck, J.B.A.P.M. De. 1792. Hedyotis. Tabl. Encycl. 1, 269-272.
51. Lau C.B.S., Cheng L., Cheng B.W.H., Yue G.G.L., Wong E.C.W., Lau C.-P., Leung P.-C., Fung K.-P. Development of a simple chromatographic method for distinguishing between two easily confused species, Hedyotis diffusa and Hedyotis corymbosa. Nat. Prod. Res. 2012, 26:1446-1450.
52. Lemmon A.R., Brown J.M., Stanger-Hall K., Lemmon E.M. The effect of ambiguous data on phylogenetic estimates obtained by maximum likelihood and Bayesian inference. Syst. Biol. 2009, 58:130-145.
53. Lewis W.H. Oldenlandia corymbosa (Rubiaceae). Grana Palynol. 1964, 5:330.
54. Lewis W.H. Pollen morphology and evolution in Hedyotis subgenus Edrisia (Rubiaceae). Am. J. Bot. 1965, 52(3):257-264.
55. Lewis W.H. The Asian genus Neanotis Nomen Novum (Anotis) and allied taxa in the Americas (Rubiaceae). Ann. Missouri Bot. Gard. 1966, 53(1):32-46.
56. Li M., Jiang R.W., Hon P.M., Cheng L., Li L.L., Zhou J.R., Shaw P.C., But P.P.-H. Authentication of the anti-tumor herb Baihuasheshecao with bioactive marker compounds and molecular sequences. Food Chem. 2010, 119:1239-1245.
57. Liang Z., He M., Fong W., Jiang Z., Zhao Z. A comparable, chemical and pharmacological analysis of the traditional Chinese medicinal herbs Oldenlandia diffusa and O. corymbosa and a new valuation of their biological potential. Phytomedicine 2008, 15:259-267.
58. Linnaeus, C., 1753. Species Plantarum. Laurentii Salvii, Stockholm, 1, 101-102, 119.
59. Löhne C., Borsch T. Molecular evolution and phylogenetic utility of the petD group II intron: a case study in basal angiosperms. Mol. Biol. Evol. 2005, 22:317-332.
60. Maddison, D.R., Maddison, W.P., 2001. MacClade: Analysis of Phylogeny and Character Evolution, Version 4.03. Sunderland, Massachusetts, Sinauer.
61. McNeill, J., Barrie, F.R., Burdet, H.M., Ddmoulin, V., Hawksworth, D.L., Marhold, K., Nicolson, D.H., Prado, J., Silva, P.C., Skog, J.E., Wiersema, J.H., Turland, N.J. (Eds.), 2006. International Code of Botanical Nomenclature (Vienna Code) adopted by the Seventeenth International Botanical Congress, Vienna, Austria, July 2005. A.R.G. Gantner Verlag KG, Ruggell (Regnum Veg. vol. 146).
62. Meisner, C.F., 1838. Pl. Vasc. Gen. (Pars Prior). Libraria Weidmannia, Lipsiae, 160.
63. Müller K. SeqState - primer design and sequence statistics for phylogenetic DNA datasets. Appl. Bioinform. 2005, 4:65-69.
64. Müller K. Incorporating information from length-mutational events into phylogenetic analysis. Mol. Phylogenet. Evol. 2006, 38:667-676.
65. Neupane S., Dessein S., Motley T.J. The Hedyotis-Oldenlandia-Kohautia complex (Rubiaceae) in Nepal: a study of fruit, seed and pollen characters and their taxonomic significance. Edinb. J. Bot. 2009, 66:371-390.
66. Nixon K.C., Carpenter J.M. On simultaneous analysis. Cladistics 1996, 12:221-242.
67. Olmstead R.G., Michaels H.J., Scotts K.M., Palmer J.D. Monophyly of the Asteridae and identification of their major lineages inferred from DNA sequences of rbcL. Ann. Missouri Bot. Gard. 1992, 79:249-265.
68. Oxelman B., Liden M., Berglund D. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst. Evol. 1997, 206:393-410.
69. Popp M., Oxelman B. Inferring the history of the polyploid Silene aegaea (Caryophyllaceae) using plastid and homoeologous nuclear DNA sequences. Mol. Phylogenet. Evol. 2001, 20:474-481.
70. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
71. Ridsdale, C.E., 1998. Rubiaceae, Tribe Hedyotideae. In: Dassanayake, M.D. (Ed.), A Revised Handbook to the Flora of Ceylon, vol. 12. A.A. Balkema, Rotterdam, pp. 236-284.
72. Rindal E., Brower A.V.Z. Do model-based phylogenetic analyses perform better than parsimony? A test with empirical data. Cladistics 2011, 27:331-334.
73. Robbrecht E. Tropical woody Rubiaceae: characteristic features and progressions: contributions to a new subfamilial classification. Opera Bot. Belg. 1988, 1:1-271.
74. Robbrecht E., Manen J.-F. The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF and atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Syst. Geogr. Plants 2006, 76:85-146.
75. Sanderson M.J., Kim J. Parametric phylogenetics?. Syst. Biol. 2000, 49:817-829.
76. Sang T., Crawford D.J., Stuessy T.F. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am. J. Bot. 1997, 84:1120-1136.
77. Sankoff D., Rousseau P. Locating the vertices of a Steiner tree in an arbitrary metric space. Math. Program. 1975, 9:240-246.
78. Schumann, K., 1891. Oldenlandia Plum. In: Engler, A., Prantl, K. (Eds.), Die Nat. Pflanzenf., vol. 4, no. 4. Verlag von Wilhelm Engelmann, Leipzig, 24-26.
79. Shi X.G., Jin J.H., Ye C.X., Liu W.Q. First fruit fossil record of Morinda (Rubiaceae) from China. Rev. Palaeobot. Palynol. 2012, 179:13-16.
80. Siddall M.E. Success of parsimony in the four-taxon case: long-branch repulsion by likelihood in the Farris Zone. Cladistics 1998, 14:209-220.
81. Simmons M.P. Independence of alignment and tree search. Mol. Phylogenet. Evol. 2004, 31:874-879.
82. Simmons M.P. Radical instability and spurious branch support by likelihood when applied to matrices with non-random distributions of missing data. Mol. Phylogenet. Evol. 2012, 62:472-484.
83. Simmons M.P., Freudenstein J.V. Spurious 99% bootstrap and jackknife support for unsupported clades. Mol. Phylogenet. Evol. 2011, 61:177-191.
84. Simmons M.P., Ochoterena H. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 2000, 49:369-381.
85. Simmons M.P., Bailey C.D., Nixon K.C. Phylogeny reconstruction using duplicate genes. Mol. Biol. Evol. 2000, 17:469-473.
86. Simmons M.P., Ochoterena H., Carr T.J. Incorporation, relative homoplasy, and effect of gap characters in sequence-based phylogenetic analyses. Syst. Biol. 2001, 50:454-462.
87. Simmons M.P., Müller K., Norton A.P. The relative performance of indel-coding methods in simulations. Mol. Phylogenet. Evol. 2007, 44:724-740.
88. Sivarajan V.V., Biju S.D. Taxonomic and nomenclatural notes on the Hedyotis corymbosa-diffusa complex (Rubiaceae) in India. Taxon 1990, 39:665-674.
89. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
90. Stamatakis, A., 2008. The RaxML 7.0.4 Manual. <> (downloaded 16.09.08). http://icwww.epfl.ch/~stamatak/index-Dateien/Page443.htm.
91. Stöver B., Müller K.F. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010, 11:7.
92. Swofford D.L. PAUP: Phylogenetic analysis using parsimony (and other methods) 2001, Sinauer, Sunderland.
93. Taberlet P., Gielly L., Pautou G., Bouvet J. Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol. Biol. 1991, 17:1105-1109.
94. Tate J.A., Simpson B.B. Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploidy species. Syst. Bot. 2003, 28:723-737.
95. Terrell E.E. Relationships of Hedyotis fruticosa L. to Houstonia L. and Oldenlandia L. Phytologia 1975, 31:418-424.
96. Terrell E.E. Stenotis (Rubiaceae), a new segregate genus from Baja California, Mexico. Sida 2001, 19:899-911.
97. Terrell E.E. Taxonomy of Stenaria (Rubiaceae: hedyotideae), a new genus including Hedyotis nigricans. Sida 2001, 19:591-614.
98. Terrell E.E., Robinson H. Survey of Asian and pacific species of Hedyotis and Exallage (Rubiaceae) with nomenclatural notes on Hedyotis types. Taxon 2003, 52:775-782.
99. Terrell E.E., Robinson H. Seed and capsule morphology in six genera of Hedyotideae (Rubiaceae): Thecagonum, Neanotis, Dentella, Kohautia, Pentodon, and Oldenlandiopsis. J. Bot. Res. Inst. Texas 2007, 1:373-384.
100. Terrell E.E., Lewis W.H., Robinson H., Nowicke J.W. Phylogenetic implications of diverse seed types, chromosome numbers, and pollen morphology in Houstonia (Rubiaceae). Am. J. Bot. 1986, 73:103-115.
101. Terrell E.E., Robinson H.E., Wagner W.L., Lorence D.H. Resurrection of Genus Kadua for Hawaiian Hedyotidinae (Rubiaceae), with emphasis on seed and fruit characters and notes on south Pacific species. Syst. Bot. 2005, 30:818-833.
102. Thulin M., Bremer B. Studies in the tribe Spermacoceae (Rubiaceae-Rubioideae): the circumscriptions of Amphiasma and Pentanopsis and the affinities of Phylohydrax. Plant Syst. Evol. 2004, 247:233-239.
103. Verdcourt B. Remarks on the classification of the Rubiaceae. Bull. Jard. Bot. Etat. Brux. 1958, 28:209-281.
104. Wang R.J., Zhao N.X. The origin and distribution on genus Hedyotis L. J. Trop. Subtrop. Bot. 2001, 9:219-228.
105. Wendel J.F., Schnabel A., Seelanan T. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc. Natl. Acad. Sci. USA 1995, 92:280-284.
106. Wight, R., Arnott, G.A.W., 1834. Prodr. Fl. Pen. Ind. Or. Parbury, Allen & Co., London, 1, 406.
107. Willdenow, C.L., 1798. Hedyotis L. Caroli à Linné species plantarum. vol. 1. G.C. Nauk., Berlin, pp. 564-568.
108. Wu X., Li A., Zhang D. Cryptic self-incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae). Plant Biol (Stuttg) 2010, 12:484-494.
109. Yang Z. Maximum-likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol. Biol. Evol. 1993, 10:1396-1401.
110. Yang Z. Computational Molecular Evolution 2006, Oxford University Press, New York.
111. Zurawski G., Clegg M.T. Evolution of higher-plant chloroplast DNA-encoded genes: implications for structure-function and phylogenetic studies. Annu. Rev. Plant Physiol. 1987, 38:391-418.