Australian Systematic Botany Australian Systematic Botany Society
Taxonomy, biogeography and evolution of plants
RESEARCH ARTICLE

Phylogeny of the holly grevilleas (Proteaceae) based on nuclear ribosomal and chloroplast DNA

Gareth D. Holmes A B C , Trisha L. Downing A , Elizabeth A. James A C , Mark J. Blacket D , Ary A. Hoffmann B and Michael J. Bayly A E

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

B Department of Genetics, Bio21 Molecular Science and Biotechnology Institute, 30 Flemington Road, The University of Melbourne, Vic. 3010, Australia.

C National Herbarium of Victoria, Royal Botanic Gardens Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia.

D Department of Environment and Primary Industries, AgriBio, La Trobe University, 5 Ring Road, Bundoora, Vic. 3083, Australia.

E Corresponding author. Email: mbayly@unimelb.edu.au

Australian Systematic Botany 27(1) 56-77 http://dx.doi.org/10.1071/SB13045
Submitted: 1 November 2013  Accepted: 8 May 2014   Published: 30 June 2014

Abstract

The holly grevilleas are an informal grouping of 15 species (19 taxa) of woody shrubs from south-eastern Australia, with a centre of distribution in central to western Victoria. Many of the species are narrowly endemic. The present study is the first molecular-phylogenetic analysis of the group, with the aim of providing an evolutionary framework for assessing species-level taxonomy and conservation priorities. Analyses using the nrDNA internal transcribed spacer (ITS) regions were complicated by the presence of divergent paralogues, including inferred pseudogenes; analyses restricted to presumed orthologous, functional ITS sequences were uninformative. Combined analyses of three chloroplast intergenic spacers (trnQ–5′rps16, trnL–trnF and rpoB–trnC) strongly support the monophyly of a core group of 16 taxa (the ‘southern holly grevilleas’) from Victoria and South Australia. However, nodes outside this group are poorly resolved and poorly supported, and the relationships of taxa from New South Wales and eastern Victoria (the ‘northern holly grevilleas’) are unclear. Among the southern holly grevilleas, the following four distinct and partly sympatric cpDNA clades are identified: the ‘Grevillea ilicifolia’, ‘G. aquifolium’, ‘G. dryophylla’ and ‘G. repens’ clades, among which the earliest and most strongly supported divergence is that of the western-most ‘G. ilicifolia’ clade. Variation in cpDNA is incongruent with current species-level taxonomy, especially for G. aquifolium (polyphyletic), G. montis-cole (polyphyletic, but the two subspecies each monophyletic) and G. microstegia (nested in G. aquifolium). The effects of incomplete chloroplast lineage sorting, gene flow through hybridisation or introgression, and inappropriate taxonomy are possible explanations for this incongruence. The formal conservation listing for some species within the holly grevillea group requires re-evaluation.

Additional keywords: Grevillea aquifolium group, holly-leaved grevilleas, ITS, molecular phylogeny, Proteaceae, rDNA pseudogenes, rpoB–trnC, taxonomy, trnL–trnF, trnQ–5′rps16.


References

Abele C, Gloe CS, Hocking JB, Holdgate GR, Kenley PR, Lawrence CR, Ripper D, Threfall WF (1976) Chapter 8: Tertiary. In ‘Geology of Victoria’. (Eds JG Douglas, JA Ferguson) Special Publication Series of The Geological Society of Australia 5, pp. 177–274. (Geological Society of Australia Incorporated: Melbourne)

Arnheim N (1983) Concerted evolution in multigene families. In ‘Evolution of Genes and Proteins’. (Eds M Nei, R Koehn) pp. 38–61. (Sinauer Associates: Sunderland, MA)

Avise JC (2004) ‘Molecular Markers, Natural History, and Evolution.’ (Sinauer Associates: Sunderland, MA)

Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molecular Phylogenetics and Evolution 29, 435–455.

Bayly MJ, Ladiges PY (2007) Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae). Molecular Phylogenetics and Evolution 44, 346–356.
Divergent paralogues of ribosomal DNA in eucalypts (Myrtaceae).CrossRef | 1:CAS:528:DC%2BD2sXmtVOltbo%3D&md5=24cc2d7757e4ed6f840b7e97983ff1a6CAS | 17188000PubMed | open url image1

Bayly MJ, Udovicic F, Gibbs AK, Parra-O. C, Ladiges PY (2008) Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis. Cladistics 24, 131–146.
Ribosomal DNA pseudogenes are widespread in the eucalypt group (Myrtaceae): implications for phylogenetic analysis.CrossRef | open url image1

Bentham G (1870) Grevillea. In ‘Flora Australiensis: A Description of the Plants of the Australian Territory. Vol. 5 (Myoporineae to Proteaceae)’. pp. 417–489. (L. Reeve & Co.: London)

Bowler JM, Hope GS, Jennings JN, Singh G, Walker D (1976) Late Quaternary climates of Australia and New Guinea. Quaternary Research 6, 359–394.
Late Quaternary climates of Australia and New Guinea.CrossRef | open url image1

Briggs JD, Leigh JH (1996) ‘Rare or threatened Australian plants.’ (CSIRO Publishing: Melbourne)

Buckler ES, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145, 821–832.

Burke JM, Bayly MJ, Adams P, Ladiges PY (2008) Molecular phylogenetic analysis of Dendrobium (Orchidaceae), with emphasis on the Australian section Dendrocoryne, and implications for generic classification. Australian Systematic Botany 21, 1–14.
Molecular phylogenetic analysis of Dendrobium (Orchidaceae), with emphasis on the Australian section Dendrocoryne, and implications for generic classification.CrossRef | 1:CAS:528:DC%2BD1cXktFyit70%3D&md5=04e5159e034585931593dc51e9056dbeCAS | open url image1

Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.CrossRef | open url image1

Byrne M, Yeates DK, Joseph L, Kearney M, Bowler J, Williams MA, Cooper S, Donnellan SC, Keogh JS, Leys R, Melville J, Murphy DJ, Porch N, Wyrwoll KH (2008) Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota.CrossRef | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=1e310eccbf8e4218d3a53861be7501f9CAS | 18761619PubMed | open url image1

Costermans LF (1981) ‘Native Trees and Shrubs of South-eastern Australia.’ (Rigby Publishers: Sydney)

Crisp MD, Laffan S, Linder HP, Monro A (2001) Endemism in the Australian flora. Journal of Biogeography 28, 183–198.
Endemism in the Australian flora.CrossRef | open url image1

D’Costa DM, Edney P, Kershaw AP, De Deckker P (1989) Late Quaternary palaeoecology of Tower Hill, Victoria, Australia. Journal of Biogeography 16, 461–482.
Late Quaternary palaeoecology of Tower Hill, Victoria, Australia.CrossRef | open url image1

Dodson JR (1974) Vegetation history and water fluctuations at Lake Leake, south-eastern South Australia. I. 10 000 B.P. to present. Australian Journal of Botany 22, 719–741.
Vegetation history and water fluctuations at Lake Leake, south-eastern South Australia. I. 10 000 B.P. to present.CrossRef | open url image1

Downing TL (2012) Investigating genetic and morphological variability in the holly grevillea Grevillea aquifolium (Proteaceae). PhD Thesis, School of Botany, The University of Melbourne.

Downing TL, Duretto MF, Ladiges PY (2004) Morphological analysis of the Grevillea ilicifolia complex (Proteaceae) and recognition of taxa. Australian Systematic Botany 17, 327–341.
Morphological analysis of the Grevillea ilicifolia complex (Proteaceae) and recognition of taxa.CrossRef | open url image1

Farris JS (1989) The retention index and homoplasy excess. Systematic Zoology 38, 406–407.
The retention index and homoplasy excess.CrossRef | open url image1

Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10, 315–319.
Testing significance of incongruence.CrossRef | open url image1

Farris JS, Källersjö M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Systematic Biology 44, 570–572.
Constructing a significance test for incongruence.CrossRef | open url image1

George AS (1998) Proteus in Australia. An overview of the current state of taxonomy of the Australian Proteaceae. Australian Systematic Botany 11, 257–266.
Proteus in Australia. An overview of the current state of taxonomy of the Australian Proteaceae.CrossRef | open url image1

Harpke D, Peterson A (2008) 5.8S motifs for the identification of pseudogenic ITS regions. Botany 86, 300–305.
5.8S motifs for the identification of pseudogenic ITS regions.CrossRef | 1:CAS:528:DC%2BD1cXltVKhs7k%3D&md5=0c81429af03ad4484ca7dcbb13b09c83CAS | open url image1

Hershkovitz MA, Zimmer EA, Hahn WJ (1999) Ribosomal DNA sequences and angiosperm systematics. In ‘Molecular Systematics and Plant Evolution’. (Eds PM Hollingsworth, RM Bateman, RJ Gornall) pp. 268–326. (Taylor and Francis: London)

Hollingsworth PM, Graham SW, Little DP (2011) Choosing and using a plant DNA barcode. PLoS ONE 6, e19254
Choosing and using a plant DNA barcode.CrossRef | 1:CAS:528:DC%2BC3MXntVajt7Y%3D&md5=986cbaec3cad31cdc9cc9daf5688d4ebCAS | 21637336PubMed | open url image1

Holmes GD (2008) Conservation biology of the rare shrub Grevillea repens F.Muell. ex Meisn. (Proteaceae). PhD Thesis, Centre for Environmental Stress and Adaption Research (CESAR; Department of Genetics) and School of Botany, The University of Melbourne.

Holmes GD, James EA, Hoffmann AA (2009) Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae). Conservation Genetics 10, 827–837.
Divergent levels of genetic variation and ploidy among populations of the rare shrub, Grevillea repens (Proteaceae).CrossRef | 1:CAS:528:DC%2BD1MXntlShu78%3D&md5=89d68098a2ffd647f849a2532f23c023CAS | open url image1

Howarth FG, James SA, McDowell W, Preston DJ, Imada CT (2007) Identification of roots in lava tube caves using molecular techniques: implications for conservation of cave arthropod faunas. Journal of Insect Conservation 11, 251–261.
Identification of roots in lava tube caves using molecular techniques: implications for conservation of cave arthropod faunas.CrossRef | open url image1

Jackson HD, Steane DA, Potts BM, Vaillancourt RE (1999) Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Molecular Ecology 8, 739–751.

James EA (2000) Implications of reproductive biology and morphology on the conservation of Grevillea williamsonii (Proteaceae). Final report to Australian Flora Foundation. Available at http://www.aff.org.au/James_Gwilliamsonii_final.pdf [Verified 22 May 2014]

James EA (2004) Conserving Grevillea williamsonii: the importance of taxonomic research for appropriate conservation action. BGjournal 1, 17–19.

James EA, McDougall KL (2014) Spatial genetic structure reflects extensive clonality, low genetic diversity and habitat fragmentation in Grevillea renwickiana (Proteaceae), a rare, sterile shrub from south-eastern Australia. Annals of Botany
Spatial genetic structure reflects extensive clonality, low genetic diversity and habitat fragmentation in Grevillea renwickiana (Proteaceae), a rare, sterile shrub from south-eastern Australia.CrossRef | 24737718PubMed | open url image1

Jobes DV, Thien LB (1997) A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences. Plant Molecular Biology Reporter 15, 326–334.
A conserved motif in the 5.8S ribosomal RNA (rRNA) gene is a useful diagnostic marker for plant internal transcribed spacer (ITS) sequences.CrossRef | 1:CAS:528:DyaK1MXjs1arurY%3D&md5=dbe02ec81129b1ed4cd94f1fe6346db4CAS | open url image1

Kelchner SA, Clark LG (1997) Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae). Molecular Phylogenetics and Evolution 8, 385–397.
Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae).CrossRef | 1:CAS:528:DyaK1cXjtVensw%3D%3D&md5=f9edcc76a21f2a57328ed8f27317fa75CAS | 9417896PubMed | open url image1

Kimpton SK, James EA, Drinnan AN (2002) Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production. Australian Systematic Botany 15, 485–492.
Reproductive biology and genetic marker diversity in Grevillea infecunda (Proteaceae), a rare plant with no known seed production.CrossRef | open url image1

Kitching IJ, Forey PL, Humphries CJ, Williams DM (1998) ‘Cladistics: The Theory and Practice of Parsimony Analysis.’ (Oxford University Press: Oxford, UK)

Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution on Anurans. Systematic Zoology 18, 1–32.
Quantitative phyletics and the evolution on Anurans.CrossRef | open url image1

Kumar S, Skjæveland Å, Orr RJS, Enger P, Ruden T, Mevik B-J, Burki F, Botnen A, Shalchian-Tabrizi K (2009) AIR: a batch-oriented web program package for construction of super matrices ready for phylogenetic analyses. BMC Bioinformatics 10, 357
AIR: a batch-oriented web program package for construction of super matrices ready for phylogenetic analyses.CrossRef | 19863793PubMed | open url image1

Liston A, Robinson WA, Oliphant JM, Alvarez-Buylla ER (1996) Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants. Systematic Botany 21, 109–120.
Length variation in the nuclear ribosomal DNA internal transcribed spacer region of non-flowering seed plants.CrossRef | open url image1

Makinson RO (1996) Grevillea. In ‘Flora of Victoria. Vol. 3’. (Eds NG Walsh, TJ Entwisle) pp. 845–870. (Inkata Press: Melbourne)

Makinson RO (2000) Grevillea. In ‘Flora of Australia. Vol. 17A: Proteaceae 2’. (Ed. AJG Wilson) pp. 1–460. (CSIRO Publishing: Melbourne)

Marginson JC, Ladiges PY (1988) Geographical variation in Eucalyptus baxteri s.l. and the recognition of a new species, E. arenacea. Australian Systematic Botany 1, 151–170.

Mast MR, Givnish TJ (2002) Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny. American Journal of Botany 89, 1311–1323.
Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny.CrossRef | 1:CAS:528:DC%2BD3sXislejsw%3D%3D&md5=978238a1894d5bba0e1f498ba5a37219CAS | open url image1

Mast AR, Willis CL, Jones EH, Downs KM, Weston PH (2008) A smaller Macadamia from a more vagile tribe: inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae). American Journal of Botany 95, 843–870.
A smaller Macadamia from a more vagile tribe: inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae).CrossRef | 21632410PubMed | open url image1

Mayol M, Roselló JA (2001) Why nuclear ribosomal spacers (ITS) tell different stories in Quercus. Molecular Phylogenetics and Evolution 19, 167–176.
Why nuclear ribosomal spacers (ITS) tell different stories in Quercus.CrossRef | 1:CAS:528:DC%2BD3MXjt1Gmsb8%3D&md5=5265945f2c243d3d6c970360587389f1CAS | 11341800PubMed | open url image1

McGillivray DJ (1986) ‘New Names in Grevillea (Proteaceae).’ (Published and distributed by the author: Sydney) [Facsimile in McGillivray and Makinson (1993)]

McGillivray DJ, Makinson RO (1993) ‘Grevillea, A Taxonomic Revision.’ (Melbourne University Press: Melbourne)

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

McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM (2001) Chloroplast sharing in the Tasmanian eucalypts. Evolution 55, 703–711.

McKinnon GE, Jordan GJ, Vaillancourt RE, Steane DA, Potts BM (2004) Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359, 275–284.

Meudt HM, Bayly MJ (2008) Phylogeographic patterns in the Australasian genus Chionohebe (Veronica s.l., Plantaginaceae) based on AFLP and chloroplast DNA sequences. Molecular Phylogenetics and Evolution 47, 319–338.
Phylogeographic patterns in the Australasian genus Chionohebe (Veronica s.l., Plantaginaceae) based on AFLP and chloroplast DNA sequences.CrossRef | 1:CAS:528:DC%2BD1cXktV2jtrc%3D&md5=272f271a0ee6137ba055560283b7b2cdCAS | 18299210PubMed | open url image1

Molyneux WM (1975) A new Grevillea species from western Victoria. Muelleria 3, 141–145.

Molyneux WM (1985) Grevillea obtecta (Proteaceae), a new species from central Victoria. Muelleria 6, 147–151.

Nelson EC (1981) Phytogeography of Southern Australia. In ‘Ecological Biogeography of Australia’, Vol. 1 (Ed. A Keast) pp. 734–759. (Dr W. Junk Publishers: The Hague, the Netherlands)

Nevill PG, Despres T, Bayly MJ, Bossinger G, Ades PK (2014) Shared phylogeographic patterns and widespread chloroplast haplotype sharing in Eucalyptus species with different ecological tolerances. Tree Genetics & Genomes
Shared phylogeographic patterns and widespread chloroplast haplotype sharing in Eucalyptus species with different ecological tolerances.CrossRef | open url image1

Olde P, Marriott N (1994) ‘The Grevillea book. Vol. 1.’ (Kangaroo Press: Sydney)

Olde P, Marriott N (1995a) ‘The Grevillea book. Vol. 2.’ (Kangaroo Press: Sydney)

Olde P, Marriott N (1995b) ‘The Grevillea book. Vol. 3.’ (Kangaroo Press: Sydney)

Pollock LJ, Bayly MJ, Nevill PG, Vesk PA (2013) Chloroplast DNA diversity associated with protected slopes and valleys for hybridizing Eucalyptus species on isolated ranges in south-eastern Australia. Journal of Biogeography 40, 155–167.
Chloroplast DNA diversity associated with protected slopes and valleys for hybridizing Eucalyptus species on isolated ranges in south-eastern Australia.CrossRef | open url image1

Rambaut A (2002) Se-Al: sequence alignment editor, version 2.0a11. Available at http://tree.bio.ed.ac.uk/software/ [Verified 22 May 2014]

Sanderson MJ, Doyle JJ (1992) Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence. Systematic Biology 41, 4–17.
Reconstruction of organismal and gene phylogenies from data on multigene families: concerted evolution, homoplasy, and confidence.CrossRef | open url image1

Sang T, Crawford DJ, Stuessy TF (1995) Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences of the United States of America 92, 6813–6817.
Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution.CrossRef | 1:CAS:528:DyaK2MXntVSksLw%3D&md5=1e2ec5a6db5d436d151bcad2d35d7128CAS | 7624325PubMed | open url image1

Schaal BA, Leverich WJ (2001) Plant population biology and systematics. Taxon 50, 679–695.
Plant population biology and systematics.CrossRef | open url image1

Schaal BA, Hayworth DA, Olsen KM, Rauscher JT, Smith WA (1998) Phylogeographic studies in plants: problems and prospects. Molecular Ecology 7, 465–474.
Phylogeographic studies in plants: problems and prospects.CrossRef | open url image1

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.
The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis.CrossRef | 1:CAS:528:DC%2BD2MXht1Klsbc%3D&md5=b689305626d9fcff7aa95c9109209391CAS | 21652394PubMed | open url image1

Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and hare III. American Journal of Botany 94, 275–288.
Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and hare III.CrossRef | 1:CAS:528:DC%2BD2sXktFOjsLg%3D&md5=e2e5ab07b9c93276ab570f470d94df24CAS | 21636401PubMed | open url image1

Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
Gaps as characters in sequence-based phylogenetic analyses.CrossRef | 1:STN:280:DC%2BD38zntlKjtg%3D%3D&md5=28e47d46829cef3c7826a15c80c9a1c4CAS | 12118412PubMed | open url image1

Smith RV (1981) A new species of Grevillea (Proteaceae) from Victoria. Muelleria 4, 423–427.

Smith RV (1983) Grevillea montis-cole sp. nov. (Proteaceae) from Victoria. Muelleria 5, 223–227.

Swofford DL (2001) ‘PAUP*. Phylogenetic analysis using parsimony, version 4.0b10.’ (Illinois Natural History Survey, Smithsonian Institution: Champaign, IL)

Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17, 1105–1109.
Universal primers for amplification of three non-coding regions of chloroplast DNA.CrossRef | 1:CAS:528:DyaK38Xhslel&md5=5ea10efc62b8cab58c7ae3beddbc4b57CAS | 1932684PubMed | open url image1

Tsitrone A, Kirkpatrick M, Levin DA (2003) A model for chloroplast capture. Evolution 57, 1776–1782.

Walsh NG, Stasjic V (2007) ‘A Census of the Vascular Plants of Victoria’, 8th edn. (Royal Botanic Gardens Melbourne: Melbourne)

White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR Protocols: A Guide to Methods and Applications’. (Eds M Innis, D Gelfand, J Sninsky, T White) pp. 315–322. (Academic Press: San Diego, CA)

Willis JH (1973) Grevillea. In ‘A Handbook to Plants in Victoria. Vol. 2: Dicotyledons’. pp. 38–48. (Melbourne University Press: Melbourne)

Wright S, Keeling J, Gillman L (2006) The road from Santa Rosalia: a faster tempo of evolution in tropical climates. Proceedings of the National Academy of Sciences of the United States of America 103, 7718–7722.
The road from Santa Rosalia: a faster tempo of evolution in tropical climates.CrossRef | 1:CAS:528:DC%2BD28XlsVGksro%3D&md5=aa9d6642fe6b371637a282dcfb814e46CAS | 16672371PubMed | open url image1


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