Advertisement

On the Relevance of Molecular Tools for Taxonomic Revision in Malvales, Malvaceae s.l., and Dombeyoideae

  • Timothée Le Péchon
  • Luc D. B. Gigord
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1115)

Abstract

In this article, we present an overview of changes to the taxonomy of Malvales. In traditional classifications, this order was variously circumscribed as including four main families (i.e., Malvaceae, Bombacaceae, Sterculiaceae, and Tiliaceae, also known now as “Core Malvales”), but major disagreements existed between different taxonomic treatments. Contributions from molecular data, new morpho-anatomical data, and progress in methodological approaches have recently led to a new broader concept of this order (namely, “expanded Malvales”). Now, expanded Malvales includes ten families (Neuradaceae, Thymelaeaceae, Sphaerosepalaceae, Bixaceae, Cistaceae, Sarcolaenaceae, Dipterocarpaceae, Cytinaceae, Muntingiaceae, Malvaceae s.l.) distributed among seven monophyletic lineages. All these families were previously considered to have malvalean affinities in some traditional treatments, except the holoparasitic and highly modified Cytinaceae. Although molecular evidence has clarified the Malvales taxonomy, the phylogenetic positions of Sarcolaenaceae, Thymelaeaceae, and Sphaerosepalaceae are still controversial and need new analyses focusing specifically on these families to assess their phylogenetic placement and their morphological evolution.

In a phylogenetic context, molecular data combined with recent examination of morphological characters supported the hypothesis of a common origin of “core Malvales.” However, these analyses also showed that the former families but Malvaceae s.s. were paraphyletic or polyphyletic. As a consequence, recent taxonomic treatments grouped taxa formerly included in “Core Malvales” in a broader concept of Malvaceae s.l. Additionally, the intrafamilial taxonomy has been deeply modified, and in its present circumscription, Malvaceae includes nine subfamilies (Grewioideae, Byttnerioideae, Sterculioideae, Dombeyoideae, Brownlowioideae, Tilioideae, Bombacoideae, Malvoideae, Helicteroideae) in two main lineages. Phylogenetic studies on subfamilial rearrangements have focused on the relationships between emblematic taxa such as Bombacoideae and Malvoideae (which form together the /Malvatheca lineage). However, our understanding of the phylogenetic relationships among and within taxa of the other subfamilies (e.g., Dombeyoideae, Tilioideae, and Sterculioideae) has not followed at the same pace. Despite recent investigations, the relationships between the subfamilies of Malvaceae s.l. remain controversial. As an example of these taxonomic issues, we review the systematic studies on Dombeyoideae, with special emphasis on taxa endemic to the Mascarene archipelago (Indian Ocean). Recent investigations have shown that several island endemic genera such as Trochetia, Ruizia, and Astiria (endemic to the Mascarenes) are nested within the mega-genus Dombeya. Consequently, the current taxonomy of this genus does not match the phylogeny and should be modified. Therefore, we propose three possible taxonomic schemes as part of an ongoing revision of the Mascarene Dombeyoideae. However, these taxonomic rearrangements should only be made after a broader study of the diversity in Madagascar and adjacent areas. This broader approach shall avoid possibly multiple and contradictory taxonomic revisions of restricted regions if they were each studied in isolation.

Key words

Taxonomy Systematics Molecular data Morphology Anatomy Phylogeny Core Malvales Dombeya Mascarenes 

Notes

Acknowledgements

This research is included in the BACOMAR Project (http://mahots.univ-reunion.fr/) supported by the University de La Réunion, the Région Réunion, the European Community, and the Ministère Français de la Recherche. Funding from the Open Laboratory of Ecological Restoration and Biodiversity Conservation of Chengdu Institute of Biology, Chinese Academy of Sciences (CAS), to Li-Bing Zhang and a CAS Research Fellowship for International Young Researchers (Grant n°31150110463) provided support to T.L.P. during the writing. We are grateful to Dr. Li-Bing Zhang and Dr. Karen Wilson for their comments on the previous version of the manuscript. We warmly thank David Caron for the illustrations and Pierre Gigord for his moral support.

References

  1. 1.
    Angiosperm Phylogeny Group (1998) An ordinal classification for the families of flowering plants. Ann MO Bot Gard 85:531–553CrossRefGoogle Scholar
  2. 2.
    Angiosperm Phylogeny Group II (2003) Classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436CrossRefGoogle Scholar
  3. 3.
    Angiosperm Phylogenetic Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121CrossRefGoogle Scholar
  4. 4.
    Judd WS, Campbell CS, Kellogg EA et al (2008) Plant systematics: a phylogenetic approach, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  5. 5.
    Cronquist A (1988) The evolution and classification of flowering plants, 2nd edn. The New York Botanical Garden, New YorkGoogle Scholar
  6. 6.
    Takhtajan A (1997) Diversity and classification of flowering plants. Columbia University Press, New YorkGoogle Scholar
  7. 7.
    Thorne RF (1992) An updated phylogenetic classification of the flowering plants. Aliso 13:365–389Google Scholar
  8. 8.
    Dahlgren G (1989) The last Dahlgrenogram: system of classification of the dicotyledons. In: Tan K, Mill RR, Elias TS (eds) Plant taxonomy, phytogeography and related subjects. Edinburgh Univ. Press, Edinburgh, pp 249–260Google Scholar
  9. 9.
    Hutchinson J (1967) The families of flowering plants. Dicotyledons, 2nd edn. Oxford University Press, LondonGoogle Scholar
  10. 10.
    Alverson WS, Karol KG, Baum DA et al (1998) Circumscription of the Malvales and relationships to other Rosidae: evidence from rbcL sequence data. Am J Bot 85:876–887PubMedCrossRefGoogle Scholar
  11. 11.
    Judd WS, Manchester SR (1997) Circumscription of Malvaceae (Malvales) as determined by a preliminary cladistic analysis of morphological, anatomical, and chemical characters. Brittonia 49:384–405CrossRefGoogle Scholar
  12. 12.
    Kubitzki K, Chase MW (2003) Introduction to Malvales. In: Kubitzki K, Bayer C (eds) V Flowering plants. Dicotyledons Malvales Capparales and non-betalain Caryophyllales. Springer, Berlin, pp 12–20CrossRefGoogle Scholar
  13. 13.
    Chase MW, Soltis DE, Olmstead RG et al (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann MO Bot Gard 80:528–548, 550–580CrossRefGoogle Scholar
  14. 14.
    Fay MF, Bayer C, Alverson WS et al (1998) Plastid rbcL sequence data indicate a close affinity between Diegodendron and Bixa. Taxon 47:43–50CrossRefGoogle Scholar
  15. 15.
    Bayer C, Fay MF, De Bruijn AY et al (1999) Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: a combined analysis of plastid atpB and rbcL DNA sequences. Bot J Linn Soc 129: 267–303Google Scholar
  16. 16.
    Nickrent DL (2007) Cytinaceae are sister to Muntingiaceae (Malvales). Taxon 56:1129–1135CrossRefGoogle Scholar
  17. 17.
    Savolainen V, Chase MW, Hoot SB et al (2000) Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Syst Biol 49:306–362PubMedCrossRefGoogle Scholar
  18. 18.
    Soltis DE, Soltis PS, Chase MW et al (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461Google Scholar
  19. 19.
    Alford MH (2006) Gerrardinaceae: a new family of African flowering plants unresolved among Brassicales, Huerteales, Malvales, and Sapindales. Taxon 55:959–964CrossRefGoogle Scholar
  20. 20.
    Soltis DE, Smith SA, Cellinese N et al (2011) Angiosperm phylogeny : 17 genes, 640 taxa. Am J Bot 98:704–730PubMedCrossRefGoogle Scholar
  21. 21.
    Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 9, June 2008Google Scholar
  22. 22.
    Nandi OI (1998) Ovule and seed anatomy of Cistaceae and related Malvanae. Plant Syst Evol 209:239–264CrossRefGoogle Scholar
  23. 23.
    Ronse Decraene LP (1989) Floral development of Cochlospermum tinctorium and Bixa orellana with special emphasis on the androecium. Am J Bot 76:1344–1359CrossRefGoogle Scholar
  24. 24.
    Jansen S, Baas P, Smets E (2000) Vestured pits in Malvales s.l.: a character with taxonomic significance hidden in the secondary xylem. Taxon 49:169–182CrossRefGoogle Scholar
  25. 25.
    Nickrent DL, Blarer A, Qiu Y-L et al (2004) Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol 4:1–17CrossRefGoogle Scholar
  26. 26.
    Ashton PS (1982) Dipterocarpaceae. In: Van Steenis CGGJ (ed) Flora Malesiana, Series 1, Spermatophyta, vol 9. Martinus Nijhoff Publishers, The Hague, pp 237–552Google Scholar
  27. 27.
    Morton CM, Dayanandan S, Dissanayake D (1999) Phylogeny and biosystematics of Pseudomonotes (Dipterocarpaceae) based on molecular and morphological data. Plant Syst Evol 216:197–205CrossRefGoogle Scholar
  28. 28.
    Maguire B, Ashton PS (1980) Pakaraimaea dipterocarpacea II. Taxon 29:225–231CrossRefGoogle Scholar
  29. 29.
    Kostermans AJGH (1978) Pakaraimaea dipterocarpacea Maguire & Ashton Belongs to Tiliaceae and Not to Dipterocarpaceae. Taxon 27:357–359CrossRefGoogle Scholar
  30. 30.
    Kostermans AJGH (1985) Family status for the Monotoideae Gilg and the Pakaraimoideae Ashton, Maguire and de Zeeuw (Dipterocarpaceae). Taxon 34:426–435CrossRefGoogle Scholar
  31. 31.
    Ducousso M, Béna G, Bourgeois C et al (2004) The last common ancestor of Sarcolaenaceae and Asian dipterocarp trees was ectomycorrhizal before the India–Madagascar separation, about 88 million years ago. Mol Ecol 13:231–236PubMedCrossRefGoogle Scholar
  32. 32.
    Dayanandan S, Ashton PS, Williams SM et al (1999) Phylogeny of the tropical tree family Dipterocarpaceae based on nucleotide sequences of the chloroplast rbcL gene. Am J Bot 86:1182–1190PubMedCrossRefGoogle Scholar
  33. 33.
    Bayer C, Chase MW, Fay MF (1998) Muntingiaceae, a new family of dicotyledons with Malvalean affinities. Taxon 47:37–42CrossRefGoogle Scholar
  34. 34.
    Bayer C (2003) Muntingiaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin, pp 315–319Google Scholar
  35. 35.
    Benn SJ, Lemke DE (1991) Taxonomy of Neotessmannieae (Tiliaceae). Am J Bot 78(Suppl):166–167Google Scholar
  36. 36.
    Carlquist S (2005) Wood and bark anatomy of Muntingiaceae: a phylogenetic comparison within Malvales s.l. Brittonia 57:59–67CrossRefGoogle Scholar
  37. 37.
    Bayer C (2003) Neuradaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin, pp 325–328Google Scholar
  38. 38.
    Ronse Decraene LP, Smets E (1995) The floral development of Neurada procumbens L. (Neuradaceae). Acta Bot Neerl 44:439–451CrossRefGoogle Scholar
  39. 39.
    Hubert H (1993) Neurada, eine Gattung der Malvales. Sendtnera 1:7–10Google Scholar
  40. 40.
    Den Outer RW, Vooren AP (1980) Bark anatomy of some Sarcolaenaceae and Rhopalocarpaceae and their systematic position. Meded Land Wagen 81:1–15Google Scholar
  41. 41.
    Gaydou EM, Ramanoelina AR (1993) A survey of the Sarcolaenaceae for cyclopropene fatty acids. Phytochemistry 22:1725–1728CrossRefGoogle Scholar
  42. 42.
    Maguire B, Ashton PS (1977) Systematic, geography and phyletic considerations. Taxon 26:343–368CrossRefGoogle Scholar
  43. 43.
    Dickison WC (1988) Xylem anatomy of Diegodendron humbertii. IAWA Bull NS 9:332–336Google Scholar
  44. 44.
    Horn JW (2004) The morphology and relationships of the Sphaerosepalaceae (Malvales). Bot J Linn Soc 144:1–40CrossRefGoogle Scholar
  45. 45.
    Beaumont AJB (2010) Systematic studies in Gnidia L. (Thymelaeaceae). Ph.D. Thesis, University of Kwazulu-Natal, South AfricaGoogle Scholar
  46. 46.
    Van der Bank M, Fay MF, Chase MW (2002) Molecular phylogenetics of Thymelaeaceae with particular reference to African and Australian genera. Taxon 51:329–339CrossRefGoogle Scholar
  47. 47.
    Herbet BE (2003) Thymelaeaceae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants. Dicotyledons. Malvales, Capparales, and non-betalain Caryophyllales. Springer, Berlin, pp 373–396Google Scholar
  48. 48.
    Corner EJH (1976) The seeds of dicotyledons, vol 1 & 2. Cambridge University Press, CambridgeGoogle Scholar
  49. 49.
    Domke W (1934) Unterschungen über die systematische und geographische Gliederung der Thymelaeaceen nebst einer Neubeschreibung ihrer Gattungen. Bibl Bot 111:1–151Google Scholar
  50. 50.
    Soltis DE, Gitzendanner MA, Soltis PS (2007) A 567-taxon data set for angiosperms: the challenges posed by Bayesian analyses of large data sets. Int J Plant Sci 168:137–157CrossRefGoogle Scholar
  51. 51.
    Wurdack KJ, Horn JW (2001) A re-evaluation of the affinities of the Tepuianthaceae: molecular and morphological evidence for placement in Malvales. Botany 2001:151 (abstract)Google Scholar
  52. 52.
    Vogel S (2000) The floral nectaries of Malvaceae sensu lato. A conspectus. Kurtziana 28:155–171Google Scholar
  53. 53.
    Alverson WS, Whitlock BA, Nyffeler R et al (1999) Phylogeny of the core Malvales: evidence from ndhF sequence data. Am J Bot 86:1474–1486PubMedCrossRefGoogle Scholar
  54. 54.
    Bayer C (1998) Synflorescences of Malvaceae. Nord J Bot 18:335–338CrossRefGoogle Scholar
  55. 55.
    Bayer C (1999) The bicolor unit—homology and transformation of an inflorescence structure unique to core Malvales. Plant Syst Evol 214:187–198CrossRefGoogle Scholar
  56. 56.
    Baum DA, Alverson WS, Nyffeler R (1998) A durian by any other name: taxonomy and nomenclature of the core Malvales. Harv Pap Bot 3:315–330Google Scholar
  57. 57.
    Whitelock BA, Bayer C, Baum DA (2001) Phylogenetic relationships and floral evolution of the Byttnerioideae (“Sterculiaceae” or Malvaceae s.l.) based on sequences of the chloroplast gene, ndhF. Syst Bot 26:420–437Google Scholar
  58. 58.
    Whitelock BA, Karol KG, Alverson WS (2003) Chloroplast DNA sequences confirm the placement of the enigmatic Oceanopapaver within Corchorus (Grewioideae: Malvaceae s.l., Formerly Tiliaceae). Int J Plant Sci 164:35–41CrossRefGoogle Scholar
  59. 59.
    Nyffeler R, Bayer C, Alverson WS et al (2005) Phylogenetic analysis of the Malvadendrina clade (Malvaceae s.l.) based on plastid DNA sequences. Org Div Evol 5:109–123CrossRefGoogle Scholar
  60. 60.
    Perveen A, Grafström E, El-Ghazaly G (2004) World Pollen and Spore Flora 23. Malvaceae Adams. P.p. Subfamilies: Grewioideae, Tilioideae, Brownlowioideae. Grana 43: 129–155CrossRefGoogle Scholar
  61. 61.
    Bayer C (2003) Malvaceae. In: Kubitzki K (ed) The families and genera of vascular plants. Springer, Berlin, pp 225–311Google Scholar
  62. 62.
    Won H (2009) Phylogenetic position of Corchoropsis Siebold & Zucc. (Malvaceae s.l.) inferred from plastid DNA sequences. J Plant Biol 52:411–416CrossRefGoogle Scholar
  63. 63.
    Barnett LC (1988) Systematics of Nesorgordonia Baillon (Sterculiaceae). Ph.D. thesis, University of Texas, AustinGoogle Scholar
  64. 64.
    Nyffeler R, Baum DA (2000) Phylogenetic relationships of the durians (Bombacaceae-Durioneae or ]Malvaceae]Helicteroideae/Durioneae) based on chloroplast and nuclear ribosomal DNA sequences. Plant Syst Evol 224:55–82CrossRefGoogle Scholar
  65. 65.
    Wilkie P, Clark A, Pennington TR et al (2006) Phylogenetic relationships within the subfamily Sterculioideae (Malvaceae/Sterculiaceae-Sterculieae) using the chloroplast gene ndhF. Syst Bot 31:160–170CrossRefGoogle Scholar
  66. 66.
    Chattaway M (1932) The wood of the Sterculiaceae. I. Specialisation of the vertical wood parenchyma within the sub-family Sterculiaceae. New Phytol 31:119–132CrossRefGoogle Scholar
  67. 67.
    Chattaway MM (1937) The wood anatomy of the family Sterculiaceae. Philos Trans Roy Soc B 228:313–365CrossRefGoogle Scholar
  68. 68.
    von Balthazar M, Schönenberger J, Alverson WS et al (2006) Structure and evolution of the androecium in the Malvatheca clade (Malvaceae s.l.) and implications for Malvaceae and Malvales. Plant Syst Evol 260:171–197Google Scholar
  69. 69.
    Baum DA, DeWitt Smith S, Yen A et al (2004) Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. Am J Bot 91:1863–1871PubMedCrossRefGoogle Scholar
  70. 70.
    von Balthazar M, Alverson WS, Schönenberger J et al (2004) Comparative floral development and androecium structure in Malvoideae (Malvaceae s.l.). Int J Plant Sci 165:445–473CrossRefGoogle Scholar
  71. 71.
    Duarte MC, Esteves GL, Salatino Maria Luiza F et al (2011) Phylogenetic Analyses of Eriotheca and Related Genera (Bombacoideae, Malvaceae). Syst Bot 36:690–701CrossRefGoogle Scholar
  72. 72.
    Skema C, Dorr LJ (2010) Dombeya gautieri (Dombeyaceae), a remarkable new species from Madagascar. Kew Bull 65:305–310CrossRefGoogle Scholar
  73. 73.
    Skema C (2012) Toward a new circumscription of Dombeya (Malvales: Dombeyaceae): a molecular phylogenetic and morphological study of Dombeya of Madagascar and a new segregate genus, Andringitra. Taxon 61:612–628Google Scholar
  74. 74.
    Thébaud C, Warren BH, Strasberg D et al (2009) Mascarene Islands, biology. In: Gillespie RG, Clague DA (eds) Encyclopedia of islands. University of California Press, Berkeley, CA, pp 612–619Google Scholar
  75. 75.
    Friedmann F (1987) Sterculiacées. In: Bosser J, Cadet T, Guého J, Marais W (eds.) Flore des Mascareignes: La Réunion, Maurice, Rodrigues. MSIRI, Port Louis, ORSTOM, Paris et Royal Botanical Garden, Kew, pp 1–50Google Scholar
  76. 76.
    Le Péchon T, Baider C, Gigord LD et al (2011) Dombeya sevathianii (Malvaceae): a new critically endangered species endemic to Mauritius (Indian Ocean). Phytotaxa 24:1–10Google Scholar
  77. 77.
    Le Péchon T, Humeau L, Gigord LDB et al (2011) Les Mahots des Mascareignes, Base de Connaissances sur les Mahots des Mascareignes. Université de La Réunion, Saint DenisGoogle Scholar
  78. 78.
    Le Péchon T, Pausé J-B, Dubuisson J-Y et al (2013) Dombeya formosa sp. nov. (Malvaceae s.l.): a New Species Endemic to La Réunion (Indian Ocean) based on morphological and molecular evidence. Syst Bot 38:424–433CrossRefGoogle Scholar
  79. 79.
    Cadet T (1980) La végétation de l'île de la Réunion: étude phytoécologique et phytosociologique. Ph.D. thesis, Université Aix-Marseilles, MarseilleGoogle Scholar
  80. 80.
    Blanchard F (2000) Guide des Milieux Naturels. La Réunion-Maurice-Rodrigues, Ulmer, ParisGoogle Scholar
  81. 81.
    Cavanilles AJ (1787) Tertia dissertatio botanica. In: Monadelphiae classis dissertations decem. Firmin-Didot et Cie, ParisGoogle Scholar
  82. 82.
    De Candolle AP (1823) Sur quelques genres nouveaux de la famille des Buttnériacées. Mém Mus Hist Nat 10:97–115Google Scholar
  83. 83.
    Lindley J (1844) Astiria rosea. In: Ridgway J (ed.) Edwards’s botanical register. London.Google Scholar
  84. 84.
    Baker JB (1877) Flora of Mauritius and the Seychelles. L. Reeve & Co., LondonGoogle Scholar
  85. 85.
    Jacob de Cordemoy E (1895) Flore de La Réunion. Klincksieck, ParisGoogle Scholar
  86. 86.
    Arènes J (1959) Les Dombeya des îles des Mascareignes. Mém Inst Sci Madagascar 9:189–216Google Scholar
  87. 87.
    Arènes J (1959) 131e Famille—Sterculiacées. In: Humbert H (ed) Flore de Madagascar et des Comores. Firmin-Didot et Cie, Paris, pp 1–537Google Scholar
  88. 88.
    Le Péchon T, Cao N, Dubuisson J-Y et al (2009) Systematics of Dombeyoideae (Malvaceae) in the Mascarene archipelago (Indian Ocean) inferred from morphology. Taxon 58:519–531Google Scholar
  89. 89.
    Le Péchon T, Haevermans T, Cruaud C et al (2010) Multiple colonizations from Madagascar and converged acquisition of dioecy in the Mascarene Dombeyoideae (Malvaceae) as inferred from chloroplast and nuclear DNA sequence analyses. Ann Bot Lond 106:343–357CrossRefGoogle Scholar
  90. 90.
    Grover CE, Salmon A, Wendel JF (2012) Targeted sequence capture as a powerful tool for evolutionary analysis. Am J Bot 99:312–319PubMedCrossRefGoogle Scholar

Copyright information

© Springer New York 2014

Authors and Affiliations

  • Timothée Le Péchon
    • 1
  • Luc D. B. Gigord
    • 2
  1. 1.Chinese Academy of SciencesChengdu Institute of BiologyChengduChina
  2. 2.Conservatoire Botanique National de MascarinSaint LeuFrance

Personalised recommendations