Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping

Molecular Phylogenetics and Evolution

Volumn 59, Issue 1, 2011, Pages 206-224

  Steane, Dorothy A ^a   Nicolle, Dean ^b   Sansaloni, Carolina P ^c,d   Petroli, César D ^c,d   Carling, Jason ^e   Kilian, Andrzej ^e   Myburg, Alexander A ^f   Grattapaglia, Dario ^c,d,g   Vaillancourt, René E ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b Currency Creek Arboretum   (Australia)

^c EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^d UNIVERSITY OF BRASILIA   (Brazil)

^e Diversity Arrays Technology Pty Ltd   (Australia)

^f UNIVERSITY OF PRETORIA   (South Africa)

^g UNIVERSIDADE CATÓLICA DE BRASÍLIA   (Brazil)

Author keywords

Australia; DArT; Diversity Arrays Technology; Molecular markers; Networks; Parsimony; Plant systematics

Indexed keywords

RIBOSOMAL SPACER DNA;

ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CLASSIFICATION; DNA MICROARRAY; EUCALYPTUS; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENETICS; GENOTYPE; HIGH THROUGHPUT SCREENING; HYBRIDIZATION; METHODOLOGY; PHYLOGENY; REPRODUCIBILITY;

BAYES THEOREM; DNA, RIBOSOMAL SPACER; EUCALYPTUS; GENETIC MARKERS; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HIGH-THROUGHPUT SCREENING ASSAYS; HYBRIDIZATION, GENETIC; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; POLYMORPHISM, GENETIC; REPRODUCIBILITY OF RESULTS;

EUCALYPTUS; EUCALYPTUS CAMALDULENSIS; EUCALYPTUS CLADOCALYX; EUCALYPTUS GLOBULUS; EUCALYPTUS GRANDIS; EUCALYPTUS NITENS; EUCALYPTUS PILULARIS; EUCALYPTUS UROPHYLLA; MYRTACEAE;

EID: 79952738006     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2011.02.003     Document Type: Article

References (104)

1. Barkley N.A., Krueger R.R., Federici C.T., Roose M.L. What phylogeny and gene genealogy analyses reveal about homoplasy in citrus microsatellite alleles. Plant Syst. Evol. 2009, 282:71-86.
2. Bayly M.J., Ladiges P.Y. Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae). Mol. Phylogenet. Evol. 2007, 44:346-356.
3. Brondani R., Brondani C., Tarchini R., Grattapaglia D. Development, characterization and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla. Theor. Appl. Genet. 1998, 97:816-827.
4. Brondani R.P.V., Williams E.R., Brondani C., Grattapaglia D. A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers from the genus. BMC Plant Biol. 2006, 6:20.
5. Brooker M.I.H. A new classification of the genus Eucalyptus L'Hér. (Myrtaceae). Aust. Syst. Bot. 2000, 13:79-148.
6. Brown A.H.D., Matheson A.C., Eldridge K.G. Estimation of mating system of Eucalyptus obliqua L'Herit. by using allozyme polymorphisms. Aust. J. Bot. 1975, 23:931-949.
7. Burgess I., Bell J.C. Comparative morphology and allozyme frequencies of Eucalyptus grandis Hill ex Maiden and Eucalyptus saligna SM. Aust. Forest Res. 1983, 13:133-149.
8. Bussell J.D., Waycott M., Chappill J.A. Arbitrarily amplified DNA markers as characters for phylogenetic inference. Perspect. Plant Ecol. Evol. Syst. 2005, 7:3-26.
9. Butcher P.A., Otero A., McDonald M.W., Moran G.F. Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia. Heredity 2002, 88:402-412.
10. Butcher P.A., McDonald M.W., Bell J.C. Congruence between environmental parameters, morphology and genetic structure in Australia's most widely distributed eucalypt, Eucalyptus camaldulensis. Tree Genet. Genomes 2009, 5:189-210.
11. Byrne M. High genetic identities between three oil mallee taxa, Eucalyptus kochii ssp. kochii, ssp. plenissima and E. horistes, based on nuclear RFLP analysis. Heredity 1999, 82:205-211.
12. Byrne M. Phylogeny, diversity and evolution of eucalypts. Plant Genome Biodiversity and Evolution. Part E. Phanerogams - Angiosperms 2008, vol. 1:303-346. Science Publishers, Berlin.
13. Byrne M., Hines B. Phylogeographical analysis of cpDNA variation in Eucalyptus loxophleba (Myrtaceae). Aust. J. Bot. 2004, 52:459-470.
14. Byrne M., Macdonald B. Phylogeography and conservation of three oil mallee taxa, Eucalyptus kochii ssp. kochii, ssp. plenissima and E. horistes. Aust. J. Bot. 2000, 48:305-312.
15. Byrne M., Marques-Garcia M.I., Uren T., Smith D.S., Moran G.F. Conservation and genetic diversity of microsatellite loci in the genus Eucalyptus. Aust. J. Bot. 1996, 44:331-341.
16. Byrne M., Parrish T.L., Moran G.F. Nuclear RFLP diversity in Eucalyptus nitens. Heredity 1998, 81:225-233.
17. Clark A.G., Hubisz M.J., Bustamante C.D., Williamson S.H., Nielsen R. Ascertainment bias in studies of human genome-wide polymorphism. Genome Res. 2005, 15:1496-1502.
18. Cook I.O., Ladiges P.Y. Isozyme variation in Eucalyptus nitens and E. denticulata. Aust. J. Bot. 1998, 46:35-44.
19. Curtu A.L., Finkeldey R., Gailing O. Comparative sequencing of a microsatellite locus reveals size homoplasy within and between European oak species (Quercus spp.). Plant Mol. Biol. Rep. 2004, 22:339-346.
20. Doyle J.J., Doyle J.L. Isolation of plant DNA from fresh tissue. Focus 1990, 12:13-15.
21. Drinnan A.N., Ladiges P.Y. Floral development and systematic position of Eucalyptus curtisii. Aust. Syst. Bot. 1991, 4:539-552.
22. Eggert L.S., Beadell J.S., McClung A., McIntosh C.E., Fleischer R.C. Evolution of microsatellite loci in the adaptive radiation of Hawaiian honeycreepers. J. Hered. 2009, 100:137-147.
23. Elliott C., Byrne M. Genetic diversity within and between natural populations of Eucalyptus occidentalis (Myrtaceae). Silvae Genet. 2003, 52:169-173.
24. Elliott C.P., Byrne M. Phylogenetics and the conservation of rare taxa in the Eucalyptus angustissima complex in Western Australia. Conserv. Genet. 2004, 5:39-47.
25. Farris J.S. The retention index and the rescaled consistency index. Cladistics 1989, 5:417-419.
26. Farris J.S., Källersjö M., Kluge A.G., Bult C. Testing significance of incongruence. Cladistics 1994, 10:315-319.
27. Forey, P.L., Humphries, C.J., Kitching, I.J., Scotland, R.W., Siebert, D.J., Williams, D.M., 1992. Cladistics. A Practical Course in Systematics. The Sytematics Association Publication No. 10. Oxford University Press, New York.
28. Freeman J.S., Jackson H.D., Steane D.A., McKinnon G.E., Dutkowski G.W., Potts B.M., Vaillancourt R.E. Chloroplast DNA phylogeography of Eucalyptus globulus. Aust. J. Bot. 2001, 49:585-596.
29. Gaiotto F.A., Bramucci M., Grattapaglia D. Estimation of outcrossing rate in a breeding program of Eucalyptus urophylla with dominant RAPD and AFLP markers. Theor. Appl. Genet. 1997, 95:842-849.
30. Gibbs A.K., Udovicic F., Drinnan A.N., Ladiges P.Y. Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology. Aust. Syst. Bot. 2009, 22:158-179.
31. Glaubitz J., Emebiri L., Moran G. Dinucleotide microsatellites from Eucalyptus sieberi: inheritance, diversity, and improved scoring of single-base differences. Genome 2001, 44:1041-1045.
32. Glaubitz J.C., Murrell J.C., Moran G.F. Effects of native forest regeneration practices on genetic diversity in Eucalyptus consideniana. Theor. Appl. Genet. 2003, 107:422-431.
33. Griffin A.R., Burgess I.P., Wolf L. Patterns of natural and manipulated hybridisation in the genus Eucalyptus L'Herit. - a review. Aust. J. Bot. 1988, 36:41-66.
34. Hill K.D., Johnson L.A.S. Systematic studies in the eucalypts. 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 1995, 6:185-504.
35. Hines B., Byrne M. Genetic differentiation between mallee and tree forms in the Eucalyptus loxophleba complex. Heredity 2001, 87:566-572.
36. Holman J.E., Hughes J.M., Fensham R.J. A morphological cline in Eucalyptus: a genetic perspective. Mol. Ecol. 2003, 12:3013-3025.
37. House A.P.N., Bell J.C. Isozyme variation and mating system in Eucalyptus urophylla ST Blake. Silvae Genet. 1994, 43:167-179.
38. House A.P.N., Bell J.C. Genetic diversity, mating system and systematic relationships in two red mahoganies, Eucalyptus pellita and E. scias. Aust. J. Bot. 1996, 44:157-174.
39. Huelsenbeck J.P., Ronquist F.R. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
40. Huson D.H. SplitsTree: a program for analyzing and visualizing evolutionary data. Bioinformatics 1998, 14:68-73.
41. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23:254-267.
42. Jaccoud D., Peng K., Feinstein D., Kilian A. Diversity arrays: a solid state technology for sequence information independent genotyping. Nucl. Acids Res. 2001, 29:e25.
43. Jackson H.D., Steane D.A., Potts B.M., Vaillancourt R.E. Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Mol. Ecol. 1999, 8:739-751.
44. James K.E., Schneider H., Ansell S.W., Evers M., Robba L., Uszynski G., Pedersen N., Newton A.E., Russell S.J., Vogel J.C., Kilian A. Diversity Arrays Technology (DArT) for pan-genomic evolutionary studies of non-model organisms. PLoS ONE 2008, 3:e1682. 10.1371/journal.pone.0001682.
45. Jones, R.C., 2009. Molecular Evolution and Genetic Control of Flowering in the Eucalyptus globulus Species Complex. PhD Thesis, University of Tasmania.
46. Jones M.E., Stokoe R.L., Cross M.J., Scott L.J., Maguire T.L., Shepherd M. Isolation of microsatellite loci from spotted gum (Corymbia variegata) and cross-species amplification in Corymbia and Eucalyptus. Mol. Ecol. Notes 2001, 1:276-278.
47. Jones M.E., Shepherd M., Henry R.J., Delves A. Chloroplast DNA variation and population structure in the widespread forest tree, Eucalyptus grandis. Conserv. Genet. 2006, 7:691-703.
48. Jones T.H., Vaillancourt R.E., Potts B.M. Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest. Mol. Ecol. 2007, 16:697-707.
49. Kress W.J., Erickson D.L. DNA barcodes: genes, genomics and bioinformatics. Proc. Natl. Acad. Sci. USA 2008, 105:2761-2762.
50. Ladiges P.Y. Phylogenetic history and classification of eucalypts. Eucalypt Ecology: Individuals to Ecosystems 1997, 16-29. Cambridge University Press, Cambridge. J.E. Williams, J.C.Z. Woinarski (Eds.).
51. Ladiges P.Y., Bayly M.J., Nelson G.J. East-west continental vicariance in Eucalyptus subgenus Eucalyptus. Beyond Cladistics: The Branching of a Paradigm 2010, 267-302. University of California. D.M. Williams, S. Knapp (Eds.).
52. Le S., Nock C., Henson M., Shepherd M. Genetic differentiation among and within three red mahoganies (ser. Annulares), Eucalyptus pellita, E. resinifera and E. scias (Myrtaceae). Aust. Syst. Bot. 2009, 22:332-343.
53. Li C.Y. RAPD analysis of genetic variation in Eucalyptus microtheca F. Muell populations. Hereditas 2000, 132:151-156.
54. Liu L., Yu L., Kubatko L., Pearl D.K., Edwards S.V. Coalescent methods for estimating phylogenetic trees. Mol. Phylogenet. Evol. 2009, 53:320-328.
55. McDonald M.W., Rawlings M., Butcher P.A., Bell J.C. Regional divergence and inbreeding in Eucalyptus cladocalyx (Myrtaceae). Aust. J. Bot. 2003, 51:393-403.
56. McDonald M.W., Brooker M.I.H., Butcher P.A. A taxonomic revision of Eucalyptus camaldulensis (Myrtaceae). Aust. Syst. Bot. 2009, 22:257-285.
57. McKinnon G.E., Vaillancourt R.E., Steane D.A., Potts B.M. The rare silver gum, Eucalyptus cordata, is leaving its trace in the organellar gene pool of Eucalyptus globulus. Mol. Ecol. 2004, 13:3751-3762.
58. McKinnon G.E., Potts B.M., Steane D.A., Vaillancourt R.E. Population and phylogenetic analysis of the cinnamoyl coA reductase gene in Eucalyptus globulus (Myrtaceae). Aust. J. Bot. 2005, 53:827-838.
59. McKinnon G.E., Vaillancourt R.E., Steane D.A., Potts B.M. An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae). Am. J. Bot. 2008, 95:368-380.
60. Moran G.F. Patterns of genetic diversity in Australian tree species. New Forests 1992, 6:49-66.
61. Mossel E., Vigoda E. Limitations of Markov Chain Monte Carlo algorithms for Bayesian inference of phylogeny. Ann. Appl. Probab. 2006, 16:2215-2234.
62. Myburg A.A., Remington D.L., O'Malley D.M., Sederoff R.R., Whetten R.W. High-throughput AFLP analysis using infrared dye-labeled primers and an automated DNA sequencer. Biotechniques 2001, 30:348-357.
63. Nesbitt K.A., Potts B.M., Vaillancourt R.E., West A.K., Reid J.B. Partitioning and distribution of RAPD variation in a forest tree species, Eucalyptus globulus. Heredity 1995, 74:628-637.
64. Nevill P.G., Reed A., Bossinger G., Vaillancourt R.E., Larcombe M., Ades P.K. Cross-species amplification of Eucalyptus microsatellite loci. Mol. Ecol. Resour. 2008, 8:1277-1280.
65. Ochieng J.W., Henry R.J., Baverstock P.R., Steane D.A., Shepherd M. Nuclear ribosomal pseudogenes resolve a corroborated monophyly of the eucalypt genus Corymbia despite misleading hypotheses at functional ITS paralogs. Mol. Phylogenet. Evol. 2007, 44:752-764.
66. Ochieng J.W., Steane D.A., Ladiges P.Y., Baverstock P.R., Henry R.J., Shepherd M. The genus Corymbia (Myrtaceae) is monophyletic at microsatellite loci. Genet. Mol. Biol. 2007, 30:1125-1134.
67. Okun D.O., Kenya E.U., Oballa P.O., Odee D.W., Muluvi G.M. Analysis of genetic diversity in Eucalyptus grandis (Hill ex Maiden) seed sources using inter simple sequence repeats (ISSR) molecular markers. Afr. J. Biotechnol. 2008, 7:2119-2123.
68. Ottewell K.M., Donnellan S.C., Moran G.F., Paton D.C. Multiplexed microsatellite markers for the genetic analysis of Eucalyptus leucoxylon (Myrtaceae) and their utility for ecological and breeding studies in other Eucalyptus species. J. Hered. 2005, 96:445-451.
69. Parra-O C., Bayly M., Udovicic F., Ladiges P. ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae). Taxon 2006, 55:653-663.
70. Payn K.G., Dvorak W.S., Janse B.J.H., Myburg A.A. Microsatellite diversity and genetic structure of the commercially important tropical tree species Eucalyptus urophylla, endemic to seven islands in eastern Indonesia. Tree Genet. Genomes 2008, 4:519-530.
71. Peakall R., Smouse P.E. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 2006, 6:288-295.
72. Perrie L.R., Shepherd L.D. Reconstructing the species phylogeny of Pseudopanax (Araliaceae), a genus of hybridizing trees. Mol. Phylogenet. Evol. 2009, 52:774-783.
73. Petroli, C.D., Sansaloni, C.P., Carling, J., Hudson, C., Steane, D.A., Myburg, A.A., Vaillancourt, R.E., Kilian, A., Grattapaglia, D., in preparation. A high-density sub-centi-Morgan DArT/microsatellite genetic linkage map for species of Eucalyptus based on 2450 markers. BMC Plant Biology.
74. Poke F.S., Martin D.P., Steane D.A., Vaillancourt R.E., Reid J.B. The impact of intragenic recombination on phylogenetic reconstruction at the sectional level in Eucalyptus when using a single copy nuclear gene (cinnamoyl CoA reductase). Mol. Phylogenet. Evol. 2006, 39:160-170.
75. Poltri S.N.M., Zelener N., Traverso J.R., Gelid P., Hopp H.E. Selection of a seed orchard of Eucalyptus dunnii based on genetic diversity criteria calculated using molecular markers. Tree Physiol. 2003, 23:625-632.
76. Posada D., Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
77. Potts B.M., Wiltshire R.J.E. Eucalypt genetics and genecology. Eucalypt Ecology: Individuals to Ecosystems 1997, 56-91. Cambridge University Press, Cambridge. J. Williams, J. Woinarski (Eds.).
78. Pryor L.D., Johnson L.A.S. A Classification of the Eucalypts 1971, Australian National University Press, Canberra.
79. Pryor L.D., Johnson L.A.S. Eucalyptus, the universal Australian. Ecological Biogeography of Australia 1981, 499-536. Dr W. Junk, The Hague. A. Keast (Ed.).
80. Ramirez M.J. Further problems with the incongruence length difference test: " hypercongruence" effect and multiple comparisons. Cladistics 2006, 22:289-295.
81. Rathbone D.A., McKinnon G.E., Vaillancourt R.E., Steane D.A., Potts B.M. Microsatellite and cpDNA variation in island and continental populations of a regionally rare eucalypt, Eucalyptus perriniana (Myrtaceae). Aust. J. Bot. 2007, 55:513-520.
82. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
83. Sale M.M., Potts B.M., West A.K., Reid J.B. Relationships within Eucalyptus using chloroplast DNA. Aust. Syst. Bot. 1993, 6:127-138.
84. Sale M.M., Potts B.M., West A.K., Reid J.B. Relationships within Eucalyptus (Myrtaceae) using PCR-amplification and southern hybridization of chloroplast DNA. Aust. Syst. Bot. 1996, 9:273-282.
85. Sansaloni C.P., Petroli C.D., Carling J., Hudson C., Steane D.A., Myburg A.A., Grattapaglia D., Vaillancourt R.E., Kilian A. A high-density Diversity Arrays Technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Meth. 2010, 6:16.
86. Shepherd M., Kasem S., Lee D., Henry R. Construction of microsatellite genetic linkage maps for Corymbia. Silvae Genet. 2006, 55:228-238.
87. Shepherd M., Kasem S., Ablett G., Ochieng J., Crawford A. Genetic structuring in the spotted gum complex (genus Corymbia, section Politaria). Aust. Syst. Bot. 2008, 21:15-25.
88. Steane D.A., West A.K., Potts B.M., Ovenden J.R., Reid J.B. Restriction fragment length polymorphisms in chloroplast DNA from six species of Eucalyptus. Aust. J. Bot. 1992, 39:399-414.
89. Steane D.A., Byrne M., Vaillancourt R.E., Potts B.M. Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae). Aust. Syst. Bot. 1998, 11:25-40.
90. Steane D.A., McKinnon G.E., Vaillancourt R.E., Potts B.M. ITS sequence data resolve higher-level relationships among the eucalypts. Mol. Phylogenet. Evol. 1999, 12:215-233.
91. Steane D.A., Vaillancourt R.E., Russell J., Powell W., Marshall D., Potts B.M. Development and characterization of microsatellite loci in Eucalyptus globulus (Myrtaceae). Silvae Genet. 2001, 50:89-91.
92. Steane D.A., Nicolle D., McKinnon G.E., Vaillancourt R.E., Potts B.M. Higher level relationships among the eucalypts are resolved by ITS-sequence data. Aust. Syst. Bot. 2002, 15:49-62.
93. Steane D.A., Conod N., Jones R.C., Vaillancourt R.E., Potts B.M. A comparative analysis of population structure of a forest tree, Eucalyptus globulus (Myrtaceae), using microsatellite markers and quantitative traits. Tree Genet. Genomes 2006, 2:30-38.
94. Steane D.A., Nicolle D., Potts B.M. Phylogenetic positioning of anomalous eucalypts by using ITS sequence data. Aust. Syst. Bot. 2007, 20:402-408.
95. Stokoe R.L., Shepherd M., Lee D.J., Nikles D.G., Henry R.J. Natural inter-subgeneric hybridisation between Eucalyptus acmenoides Schauer and Eucalyptus cloeziana F. Muell (Myrtaceae) in southeast Queensland. Ann. Bot. 2001, 88:563-570.
96. Swofford, D.L., 1999. 'PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods), Version 4. Sinauer, Sunderland, MA.
97. Thamarus K.A., Groom K., Murrel J., Byrne M., Moran G.F. A genetic linkage map for Eucalyptus globulus with candidate loci for wood, fibre and floral traits. Theor. Appl. Genet. 2002, 104:379-387.
98. Udovicic F., McFadden G., Ladiges P.Y. Phylogeny of Eucalyptus and Angophora based on 5S rDNA spacer sequence DNA. Mol. Phylogenet. Evol. 1995, 4:247-256.
99. Vekemans, X., 2002. AFLP-SURV Version 1.0. Distibuted by the Author, Laboratoire de Genetique et Ecologie Vegetale, Universite Libre de Bruxelles, Belgium.
100. Walker E., Byrne M., Macdonald B., Nicolle D., McComb J. Clonality and hybrid origin of the rare Eucalyptus bennettiae (Myrtaceae) in Western Australia. Aust. J. Bot. 2009, 57:180-188.
101. Wheeler M.A., Byrne M. Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia. Aust. J. Bot. 2006, 54:17-26.
102. Wheeler M.A., Byrne M., McComb J.A. Little genetic differentiation within the dominant forest tree, Eucalyptus marginata (Myrtaceae) of South-Western Australia. Silvae Genet. 2003, 52:254-259.
103. Whittock S., Steane D.A., Vaillancourt R.E., Potts B.M. Molecular evidence shows that the tropical boxes (Eucalyptus subgenus Minutifructus) are over-ranked. Trans. Roy. Soc. S. Aust. 2003, 127:27-32.
104. Wright I.J., Ladiges P.Y. Geographic variation in Eucalyptus diversifolia (Myrtaceae) and the recognition of new subspecies E. Diversifolia subsp. hesperia and E. diversifolia subsp. megacarpa. Aust. Syst. Bot. 1997, 10:651-680.