Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology

Adele K. Gibbs; Frank Udovicic; Andrew N. Drinnan; Pauline Y. Ladiges

doi:10.1071/SB08043

RESEARCH ARTICLE

Previous Next Contents Vol 22(3)

Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology

Adele K. Gibbs ^A , Frank Udovicic ^B , Andrew N. Drinnan ^A and Pauline Y. Ladiges ^A ^C

+ Author Affiliations

- Author Affiliations

^A School of Botany, The University of Melbourne, Vic. 3010, Australia.

^B Royal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia.

^C Corresponding author. Email: p.ladiges@unimelb.edu.au

Australian Systematic Botany 22(3) 158-179 https://doi.org/10.1071/SB08043
Submitted: 11 September 2008 Accepted: 24 February 2009 Published: 10 June 2009

Abstract

Phylogenetic analysis of Eucalyptus subgenus Eudesmia is presented on the basis of the following three datasets: sequences of the internal transcribed spacer (ITS) and the external transcribed spacer (ETS) regions from nuclear rDNA, sequences of the psbA–trnH intergenic spacer region from chloroplast DNA, and morphological characters, including stamen bundling, operculum development, seeds and trichomes. Studies of floral development were essential for understanding the morphology of mature flowers and interpretation of synapomorphy and homoplasy. A summary phylogeny was constructed from a maximum parsimony analysis of those nodes coded as characters that had support in the molecular trees together with morphological characters. A revised infra-subgeneric classification is presented on the basis of the summary phylogeny, and compared with classifications of Hill and Johnson (1998) and Brooker (2000). Differences relate to relationships between clades and taxonomic rank (sections, series and subseries) and valid names of Brooker (2000) are conserved where possible. One main clade of 14 species (section Limbatae), many of mallee growth form, was found in all analyses; this clade is distributed in the South-West of Western Australia and adjacent Interzone and desert areas. A second main clade (section Complanatae) occurs in the northern and eastern tropical and subtropical regions of Australia, including Kimberley, Arnhem, Queensland and New South Wales. This section includes E. tetrodonta, previously treated as an isolated taxon in a monotypic section; however, this species is related to E. baileyana, E. similis, E. lirata and series Miniatae. The hypothesised phylogeny provides a framework for further analyses of biogeography and ecology, including functional traits.

Acknowledgements

Dean Nicolle, Marjorie King, Royal Botanic Gardens Sydney Seedbank, and Kings Park and Botanic Gardens provided plant material and seeds. Wayne Gebert and Neville Walsh provided Latin diagnoses. This work was funded by ARC Linkage Grant LP0455375, with support from Royal Botanic Gardens Melbourne, and Maud Gibson Trust. AG was supported by the Hansjörg Eichler Scientific Research Award (Australian Systematic Botany Society), a Melbourne Research Scholarship, the Ethel McLennan Award (The Botany Foundation) and an Albert Shimmin Award, Faculty of Science, University of Melbourne.

References

Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and ITS trees of Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10, 449–463.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Bayly MJ, Ladiges PY (2007) Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae). Molecular Phylogenetics and Evolution 44, 346–356.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Bayly MJ, Udovicic F, Gibbs AK, Parra-O. C, Ladiges PY (2008) Ribosomal DNA pseudogenes are widespread in eucalypts (Myrtaceae): implications for phylogenetic analysis. Cladistics 24, 131–146.
| Crossref | GoogleScholarGoogle Scholar |

Bean AR (2006) Eucalyptus megasepala A.R.Bean (Myrtaceae), a new species from Queensland allied to E. tetrodonta F.Muell. Austrobaileya 7, 305–310.

Bentham G (1867) ‘Flora Australiensis.’ (Reeve: London)

Blakely WF (1934) ‘A key to eucalypts.’ (Forestry and Timber Bureau: Canberra)

Bohte A, Drinnan AN (2005) Ontogeny, anatomy and systematic significance of ovular structures in the ‘eucalypt group’ (Eucalyptae, Myrtaceae). Plant Systematics and Evolution 255, 17–39.
| Crossref | GoogleScholarGoogle Scholar |

Boland DJ , Brooker MIH , Turnbull JW , Kleinig DA (1980) ‘Eucalyptus seed.’ (CSIRO: Melbourne)

Brooker MIH (2000) A new classification of the genus Eucalyptus L’Hér. (Myrtaceae). Australian Systematic Botany 13, 79–148.
| Crossref | GoogleScholarGoogle Scholar |

Brown R (1814) In ‘A voyage to Terra Australis, Vol. 2’. (Ed. M Flinders) p. 599. (G. and W. Nicol: London)

Brown GK, Craven LA, Udovicic F, Ladiges PY (2006) Phylogeny of Rhododendron section Vireya (Ericaceae) based on two non-coding regions of cpDNA. Plant Systematics and Evolution 257, 57–93.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Carr SGM, Carr DJ (1968) Operculum development and the taxonomy of eucalypts. Nature 219, 513–515.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Chippendale GM (1988) ‘Eucalyptus, Angophora, Vol. 19.’ (Australian Government Publishing Service: Canberra)

Drinnan AN, Ladiges PY (1989a) Corolla and androecium development in some Eudesmia eucalypts (Myrtaceae). Plant Systematics and Evolution 165, 239–254.
| Crossref | GoogleScholarGoogle Scholar |

Drinnan AN, Ladiges PY (1989b) Operculum development in Eucalyptus cloeziana and Eucalyptus informal subg. Monocalyptus (Myrtaceae). Plant Systematics and Evolution 166, 183–196.
| Crossref | GoogleScholarGoogle Scholar |

Drinnan AN, Ladiges PY (1989c) Operculum development in the Eudesmieae B eucalypts and Eucalyptus caesia (Myrtaceae). Plant Systematics and Evolution 165, 227–237.
| Crossref | GoogleScholarGoogle Scholar |

Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of congruence. Cladistics 10, 315–319.
| Crossref | GoogleScholarGoogle Scholar |

Gardiner-Garden M, Sved JA, Frommer M (1992) Methylation sites in angiosperm genes. Journal of Molecular Evolution 34, 219–230.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Gauba E, Pryor LD (1959) Seed coat anatomy and taxonomy in Eucalyptus 2. Proceedings of the Linnean Society of New South Wales 84, 278–291.

Gauba E, Pryor LD (1961) Seed coat anatomy and taxonomy in Eucalyptus 3. Proceedings of the Linnean Society of New South Wales 86, 96–111.

Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| CAS |

Hallam ND, Chambers TC (1970) The leaf waxes of the genus Eucalyptus L’Heritier. Australian Journal of Botany 18, 335–386.
| Crossref | GoogleScholarGoogle Scholar |

Hershkovitz MA, Lewis LA (1996) Deep-level diagnostic value of the rDNA-ITS region. Molecular Biology and Evolution 13, 1276–1295.
| CAS | PubMed |

Hill KD, Johnson LAS (1998) Systematic studies in the eucalypts. 8. A review of the eudesmioid eucalypts, Eucalyptus subgenus Eudesmia (Myrtaceae). Telopea 7, 375–414.

Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Huelsenbeck JP, Larget B, Miller RE, Ronquist F (2002) Potential applications and pitfalls of Bayesian inference of phylogeny. Systematic Biology 51, 673–688.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Käss E, Wink M (1997) Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1 + 2 regions of rDNA. Plant Systematics and Evolution 208, 139–167.
| Crossref | GoogleScholarGoogle Scholar |

Ladiges PY (1984) A comparative study of trichomes in Angophora Cav. and Eucalyptus L’Hérít. – a question of homology. Australian Journal of Botany 32, 561–574.
| Crossref | GoogleScholarGoogle Scholar |

Ladiges PY, Udovicic F, Drinnan AN (1995) Eucalypt phylogeny – molecules and morphology. Australian Systematic Botany 8, 483–497.
| Crossref | GoogleScholarGoogle Scholar |

Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution 16, 750–759.
| CAS |

Lucas E, Harris SA, Mazine FF, Belsham SR, Lughadha N, Eimear M, Telford A, Gasson PE, Chase MW (2007) Suprageneric phylogenetics of Myrteae, the generically richest tribe in Myrtaceae (Myrtales). Taxon 56, 1105–1128.

Maiden JH (1903–1931) ‘A critical revision of the genus Eucalyptus.’ (Government Printer: Sydney)

Martins L, Hellwig FH (2005) Systematic position of the genera Serratula and Klasea within Centaureinae (Cardueae, Asteraceae) inferred from ETS and ITS sequence data and new combinations in Klasea. Taxon 54, 632–638.

McKinnon GE, Steane DA, Potts BM, Vaillancourt RE (1999) Incongruence between chloroplast species phylogenies in Eucalyptus subgenus Monocalyptus (Myrtaceae). American Journal of Botany 86, 1038–1046.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Mueller Fv (1879–1884) ‘Eucalyptographia. A descriptive atlas of the eucalypts of Australia and the adjoining islands.’ (Government Printer: Melbourne)

Nicolle D (2000) Three new taxa of Eucalyptus subgenus Eudesmia (Myrtaceae) from Queensland and Western Australia. Nuytsia 13, 317–329.

Nicolle D (2003) ‘Currency Creek Arboretum. Eucalypt research, Vol. 2.’ (D. Nicolle: Adelaide)

Ochieng JW, Henry RJ, Baverstock PR, Steane DA, Shepherd M (2007) Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogues. Molecular Phylogenetics and Evolution 44, 752–764.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Parra-O. C, Bayly M, Udovicic F, Ladiges P (2006) ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae). Taxon 55, 653–663.

Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.
| Crossref | GoogleScholarGoogle Scholar | PubMed |

Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Pryor LD , Johnson LAS (1971) ‘A classification of the eucalypts.’ (Australian National University: Canberra)

Ronquist F , Huelsenbeck JP , van der Mark P (2005) ‘MrBayes 3.1 Manual.’ Available at http://mrbayes.csit.fsu.edu/mb3.1_manual.pdf

Sale MM, Potts BM, West AK, Reid JB (1993) Relationships within Eucalyptus using chloroplast DNA. Australian Systematic Botany 6, 127–138.
| Crossref | GoogleScholarGoogle Scholar |

Sale MM, Potts BM, West AK, Reid JB (1996) Relationships within Eucalyptus (Myrtaceae) using PCR amplification and southern hybridisation of chloroplast DNA. Australian Systematic Botany 9, 273–282.
| Crossref | GoogleScholarGoogle Scholar |

Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120–1136.
| CAS | Crossref |

Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92, 142–166.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Steane DA, McKinnon GE, Vaillancourt RE, Potts BM (1999) ITS sequence data resolve higher level relationships among the eucalypts. Molecular Phylogenetics and Evolution 12, 215–223.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Steane DA, Nicolle D, McKinnon GE, Vaillancourt RE, Potts BM (2002) Higher-level relationships among the eucalypts are resolved by ITS-sequence data. Australian Systematic Botany 15, 49–62.
| Crossref | GoogleScholarGoogle Scholar |

Swofford DL (2002) ‘PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4.’ (Sinauer Associates: Sunderland, MA)

Udovicic F, Ladiges PY (2000) Informativeness of nuclear and chloroplast DNA regions and the phylogeny of the eucalypts and related genera (Myrtaceae). Kew Bulletin 55, 633–645.
| Crossref | GoogleScholarGoogle Scholar |

Udovicic F, Murphy DJ (2002) Successful DNA amplification from Acacia (Leguminosae) and other refractory Australian plants and fungi using a nested/semi-nested PCR protocol. Muelleria 16, 47–53.

Udovicic F, McFadden GI, Ladiges PY (1995) Phylogeny of Eucalyptus and Angophora based on 5S rDNA spacer sequence DNA. Molecular Phylogenetics and Evolution 4, 247–256.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Whittock S, Steane DA, Vaillancourt RE, Potts BM (2003) Molecular evidence shows that the tropical boxes (Eucalyptus subgenus Minutifructus) are over-ranked. Transactions of the Royal Society of South Australia 127, 27–32.

Wilcox TP, Zwickl DJ, Heath TA, Hillis DM (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution 25, 361–371.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Wiley EO (1981) ‘Phylogenetics: the theory and practice of phylogenetic systematics.’ (John Wiley & Sons: New York)

Wright SD, Yong CG, Wichman SR, Dawson JW, Gardner RC (2001) Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS + ETS). Journal of Biogeography 28, 769–774.
| Crossref | GoogleScholarGoogle Scholar |

**Appendix 1. DNA sources or published sequences used in analyses (shown here in bold), wet collections of flower buds and examples of voucher specimens examined for morphology**
AB, A. Bohte; AD, Adelaide Herbarium; AG, A. Gibbs; AND, A. N. Drinnan; CANB, Canberra Herbarium; CCA, Currency Creek Arboretum, South Australia; CL, Cookson Laboratory, The University of Melbourne; CSIRO, Commonwealth Scientific and Industrial Research Organisation, Australian Tree Seed Centre; FRI, CSIRO Division of Forest Research, Yarralumla; KPBG, Kings Park and Botanic Gardens, Perth; MELU, The University of Melbourne Herbarium; MIHB, M. I. H. Brooker; NSW, New South Wales; NT, Northern Territory; PYL, P. Y. Ladiges; Qld, Queensland; RBG, Syd., Royal Botanic Gardens, Sydney; SA, South Australia; Vic., Victoria; WA, Western Australia. Subgenera are according to Brooker (2000). For the Currency Creek material, vouchers numbers (DN#) are those of D. Nicolle and are for the parent tree from which first generation offspring were grown (see Nicolle 2003)