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

An assessment of old and new DNA sequence evidence for the paraphyly of Banksia with respect to Dryandra (Proteaceae)

Austin R. Mast A B , Eric H. Jones A and Shawn P. Havery A
+ Author Affiliations
- Author Affiliations

A Department of Biological Science, Florida State University, Tallahassee, Florida 32306, USA.

B Corresponding author. Email: Amast@bio.fsu.edu

Australian Systematic Botany 18(1) 75-88 https://doi.org/10.1071/SB04015
Submitted: 3 June 2004  Accepted: 31 December 2004   Published: 29 March 2005

Abstract

Banksia (80 spp.; Proteaceae) has undergone extensive speciation and adaptive radiation on the island continent of Australia. Its members range from prostrate shrubs in the dry, infertile sandplains to 25 m tall trees in the loams of river margins, and they display striking variation in their fire survival strategies and floral and foliar morphologies. We examine the weight of both previously published (most trnL intron, trnL/F spacer, and rpl16 intron data) and new (matK, atpB, and waxy data, as well as most ITS data) DNA sequence evidence for the paraphyly of Banksia with respect to a monophyletic Dryandra (93 spp.). The nuclear waxy gene appears to be at two loci in the Proteaceae, and sequences presumably from the same locus resolve Banksia as paraphyletic with respect to Dryandra. The waxy and combined chloroplast DNA (cpDNA) data reject the monophyly of Banksia at a threshold of P = 0.05 using the winning sites and Kishino–Hasegawa tests. We consider this result and the repeated placement of Dryandra in the same clade (/Cryptostomata) of Banksia with each separate analysis of the DNA datasets (cpDNA, ITS, and waxy), to be strong molecular support for the paraphyly of Banksia with respect to Dryandra. The morphological synapomorphy of beaked follicles for /Cryptostomata (including Dryandra) reinforces this conclusion. We argue that realignment of taxa to produce one or more monophyletic genera is best attained by moving the taxa of Dryandra to Banksia. This would produce an easily recognised genus Banksia with four morphological synapomorphies. It would also probably confer some of the research attention garnered by the adaptive radiation of Banksia to the under-studied taxa of Dryandra, for Dryandra makes the radiation of Banksia even more remarkable.


Acknowledgments

We thank the organisers of this special issue of Australian Systematic Botany for the invitation to submit a manuscript and two anonymous reviewers for their helpful comments. Roberta Mason-Gamer suggested useful primer annealing sites for the waxy gene. D Sky Feller and Don Williams helped in the field, and Deborah Paul helped with GenBank submissions. The Florida State University (FSU) Department of Biological Science, College of Arts and Science, and Office of Research generously provided support for the project through the start-up budget of ARM. EJ was supported by an FSU Council on Research and Creativity Planning Grant to ARM.


References


Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Annals of the Missouri Botanical Garden 82, 247–277. open url image1

Baum DA, Alverson WS, Nyffeler R (1998a) A durian by any other name: taxonomy and nomenclature of the core Malvales. Harvard Papers in Botany 3, 315–330. open url image1

Baum DA, Small RL, Wendel JF (1998b) Biogeography and floral evolution of baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets. Systematic Biology 47, 181–207.
CrossRef | PubMed | open url image1

Beard JS, Chapman AR, Gioia P (2000) Species richness and endemism in the Western Australian flora. Journal of Biogeography 27, 1257–1268.
CrossRef | open url image1

Brown R (1810) Dryandra. Transactions of the Linnean Society of London 10, 211–215. open url image1

Buckler ES, Ippolito A, Holtsford TP (1997) The evolution of ribosomal DNA: divergent paralogues and phylogenetic implications. Genetics 145, 821–832.
PubMed |
open url image1

Cantino, PD ,  and  de Queiroz, K (2003). ‘Phylocode: a phylogenetic code of biological nomenclature. Version 2a.’ Published electronically at 10 January 2005. http://www.ohiou.edu/phylocode/validated

Carlquist, SJ (1974). ‘Island biology.’ (Columbia University Press: New York)

Carpenter RJ, Jordan GJ, Hill RS (1994) Banksieaephyllum taylorii (Proteaceae) from the Late Paleocene of New South Wales and its relevance to the origin of Australia’s scleromorphic flora. Australian Systematic Botany 7, 385–392. open url image1

Evans RC, Alice LA, Campbell CS, Kellogg EA, Dickinson TA (2000) The granule-bound starch synthase (GBSSI) gene in the Rosaceae: multiple loci and phylogenetic utility. Molecular Phylogenetics and Evolution 17, 388–400.
CrossRef | PubMed | open url image1

Farris JS (1989) The retention index and the rescaled consistency index. Cladistics 5, 417–419. open url image1

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

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791. open url image1

George AS (1981) The genus Banksia L.f. (Proteaceae). Nuytsia 3, 239–473. open url image1

George AS (1996) New taxa and a new infrageneric classification in Dryandra R.Br. (Proteaceae: Grevilleoideae). Nuytsia 10, 313–408. open url image1

George, AS (1999a). Banksia. In ‘Flora of Australia. Vol. 17B. Proteaceae 3. to ’. a. pp. 175–251. (CSIRO Publishing: Melbourne)

George, AS (1999b). Dryandra. In ‘Flora of Australia. Vol. 17B. Proteaceae 3. to ’. b. pp. 251–263. (CSIRO Publishing: Melbourne)

Greuter, W , McNeill, J , Barrie, FR , Burdet, HM , Demoulin, V , Filgueiras, TS , Nicolson, DH , Silva, PC , Skog, JE , Trehane, P , Turland, NJ ,  and  Hawksworth, DL (2000). ‘International code of botanical nomenclature (St Louis Code).’ (Koeltz Scientific Books: Königstein)

Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 21, 160–174. open url image1

Hilu KW, Borsch T, Müller K, Soltis DE, Soltis PS , et al. (2003) Angiosperm phylogeny based on matK sequence information. American Journal of Botany 90, 1758–1776. open url image1

Hopper, SD (1992). Patterns of plant diversity at the population and species levels in south-west Australian mediterranean ecosystems. In ‘Biodiversity of mediterranean ecosystems in Australia’. pp. 27–46. (Surrey Beatty and Sons: Sydney)

Hoot SB, Culham A, Crane PR (1995) The utility of atpB gene sequences in resolving phylogenetic relationships: comparisons with rbcL and 18S ribosomal DNA sequences in the Lardizabalaceae. Annals of the Missouri Botanical Garden 82, 194–208. open url image1

Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.
CrossRef | PubMed | open url image1

Johnson LA, Soltis DE (1994) MatK DNA sequences and phylogenetic reconstruction in Saxifragaceae s.str. Systematic Botany 19, 143–156. open url image1

Johnson LAS, Briggs BG (1975) On the Proteaceae—the evolution and classification of a southern family. Botanical Journal of the Linnean Society 70, 83–182. open url image1

Jordan WCM, Courtney W, Neigel JE (1996) Low levels of intraspecific genetic variation at a rapidly evolving chloroplast DNA locus in North American duckweeds (Lemnaceae). American Journal of Botany 83, 430–439. open url image1

Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution 29, 170–179.
PubMed |
open url image1

Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Systematic Zoology 18, 1–32. open url image1

Lamont, BB (1996). Conservation biology of banksias in southwestern Australia. In ‘Gondwanan heritage: past, present and future of the Western Australian biota’. pp. 292–298. (Surrey Beatty: Sydney)

Lamont BB, Connell SW (1996) Biogeography of Banksia in southwestern Australia. Journal of Biogeography 23, 295–309.
CrossRef | open url image1

Lamont BB, Markey A (1995) Biogeography of fire-killed and resprouting Banksia species in south-western Australia. Australian Journal of Botany 43, 283–303. open url image1

Lanave C, Preparata G, Saccone C, Serio G (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution 20, 86–93.
PubMed |
open url image1

Linneaus, C (1781). ‘Supplementum Plantarum systematis vegetabilium’. (Brunsvigae: Orphanotrophei)

Maguire TL, Conran JG, Collins GG, Sedgley M (1997) Molecular analysis of interspecific and intergeneric relationships of Banksia using RAPDs and non-coding chloroplast DNA sequences. Theoretical and Applied Genetics 95, 253–260.
CrossRef | open url image1

Mason-Gamer RJ, Weil CR, Kellogg EA (1998) Granule-bound starch synthase: structure, function, and phylogenetic utility. Molecular Biology and Evolution 15, 1658–1673.
PubMed |
open url image1

Mast AR (1998) Molecular systematics of subtribe Banksiinae (Banksia and Dryandra; Proteaceae) based on cpDNA and nrDNA sequence data: implications for taxonomy and biogeography. Australian Systematic Botany 11, 321–342.
CrossRef | open url image1

Mast AR (2000) Molecular systematics of the subtribe Banksiinae (Banksia and Dryandra; Proteaceae), with insights into the historical biogeography of Australia and the origin of xeromorphic leaf traits. PhD thesis. (University of Wisconsin: Madison, WI)

Mast AR, 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. open url image1

Mickevich MF, Farris JS (1981) The implications of congruence in Menidia.  Systematic Zoology 30, 351–370. open url image1

Mullis KB, Faloona FA (1987) Specific synthesis of DNA in vitro via a polymerase catalyzed chain reaction. Methods in Enzymology 155, 335–350.
PubMed |
open url image1

Orchard, AE (1999). Introduction. In ‘Flora of Australia. Vol. 1. Introduction’. (2nd edn) pp. 1–10. (CSIRO Publishing: Melbourne)

Pieroni M, George AS (1996) Illustrated key to Dryandra. Dryandra Study Group Newsletter 30, 1–19. open url image1

Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
CrossRef | PubMed | open url image1

Prager EM, Wilson AC (1988) Ancient origin of lactalbumin from lysozyme: analysis of DNA and amino acid sequences. Journal of Molecular Evolution 27, 326–335.
PubMed |
open url image1

Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.
PubMed |
open url image1

Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84, 1120–1136. open url image1

Soltis, DE ,  and  Soltis, PS (1998). Choosing an approach and an appropriate gene for phylogenetic analysis. In ‘Molecular systematics of plants II: DNA sequencing’. pp. 1–42. (Kluwer Academic Publishers: Boston)

Swofford, DL (2002). ‘PAUP*. Phylogenetic analysis using parsimony (* and other methods). Version 4b10.’ (Sinauer Associates: Sunderland: MA)

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.
CrossRef | PubMed | open url image1

Tavare S (1986) Some probabilistic and statistical problems on the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17, 57–86. open url image1

Taylor, A ,  and  Hopper, SD (1988). ‘The atlas.’ (Australian Government Publishing Service: Canberra)

Thiele K, Ladiges PY (1996) A cladistic analysis of Banksia (Proteaceae). Australian Systematic Botany 9, 661–733. open url image1

Van Der Leij FR, Visser RG, Ponstein AS, Jacobsen E, Feenstra WJ (1991) Sequence of the structural gene for granule-bound starch synthase of potato (Solanum tuberosum L.) and evidence for a single point deletion in the amf allele. Molecular Gene Genetics 228, 240–248. open url image1

Venkata Rao C (1964) Studies in the Proteaceae IV. Tribes Banksieae, Musgraveae and Embothrieae. Proceedings of the National Institute of Science of India. Series B 30, 197–244. open url image1

White, TJ , Bruns, T , Lee, S ,  and  Taylor, J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR protocols: a guide to methods and applications’. pp. 315–322. (Academic Press: San Diego)

Witkowski ETF, Lamont BB, Walton CS, Radford S (1992) Leaf demography, sclerophylly and ecophysiology of two banksias with contrasting leaf life spans. Australian Journal of Botany 40, 849–862. open url image1

Yang Z (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution 39, 306–314.
CrossRef | PubMed | open url image1








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