Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology

A molecular phylogeny of the Australian monitor lizards (Squamata : Varanidae) inferred from mitochondrial DNA sequences

A. J. Fitch A B C , A. E. Goodman A and S. C. Donnellan B

A School of Biological Sciences, Flinders University, GPO Box 2100, SA 5001, Australia.

B Evolutionary Biology Unit and Centre for Evolutionary Biology and Biodiversity, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

C Corresponding author. Email:

Australian Journal of Zoology 54(4) 253-269
Submitted: 11 July 2005  Accepted: 9 May 2006   Published: 11 August 2006


To date no complete phylogeny of all of the currently recognised Indo-Australian varanid species and subspecies has been published. This paper presents a comprehensive mitochondrial gene phylogeny of these lizards. A portion of the mitochondrial genome comprising part of the ND4 gene and three adjacent tRNA genes (hereafter referred to as ND4) was analysed alone and, for a subset of the taxa, combined with previously published mitochondrial data. Similar tree topologies were produced by both datasets although combining the data helped resolve some of the unresolved or weakly supported nodes in the ND4 analyses. The monophyly of the Indo-Australian group was strongly supported in all analyses. This group comprised three major lineages: the gouldii group, the Odatria group and the varius group. Mitochondrial ND4 nucleotide sequences were successfully amplified from all of the Indo-Australian monitor species and subspecies currently recognised and, as such, is the first comprehensive phylogenetic study of the Australian monitor lizards published. Analysis of the tempo of diversification and evolution of preferred habitat use identified six episodes of increased net speciation rate, with two closely adjacent episodes showing the highest rates of diversification and correlating with the appearance of all preferred habitat types. The comprehensive molecular phylogenetic framework will also be useful for the identification of varanid species and traded products derived from monitors and, as such, has important applications for wildlife management and conservation.


Arévalo E. Davis S. K. Sites J. Jr 1994 Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in Central Mexico. Systematic Biology 43 387 418

Ast J. C. 2001 Mitochondrial DNA evidence and evolution in Varanoidea (Squamata). Cladistics 17 211 226

Banks M. A. Hedgecock D. Waters C. 1993 Discrimination between closely related Pacific oyster species (Crassostrea) via mitochondrial DNA sequences coding for large subunit rRNA. Molecular Marine Biology and Biotechnology 2 129 136

Barraclough T. G. Nee S. 2001 Phylogenetics and speciation. Trends in Ecology & Evolution 16 391 399

Bartlett S. E. Davidson W. S. 1992 FINS (Forensically Informative Nucleotide Sequencing): a procedure for identifying the animal origin of biological specimens. BioTechniques 12 408 411

Baverstock P. B. King D. King M. Birrell J. Krieg M. 1993 The evolution of species of the Varanidae: microcomplement fixation analysis of serum albumins. Australian Journal of Zoology 41 621 638

Becker H. O. 1991 The lung morphology of Varanus yemenensis Böhme, Joger and Schätti, 1989, and its bearing on the systematics of the Afro-Asian monitor radiation. Mertensiella 2 29 37

Becker H. O. Böhme W. Perry S. F. 1989 Die Lungenmorphologie der Warane (Reptilia: Varanidae) und ihre Systematisch-stammesgeschichtliche Bedeutung. Bonner Zoologische Beiträge, Bonn 40 27 56

Besansky N. J. Severson D. W. Ferdig M. T. 2003 DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you. Trends in Parasitology 19 545 546

Böhme W. 1988 Zur Genitalmorphologie der Sauria: funktionelle und stammesgeschichtliche Aspekte. Bonner Zoologische Monographien 27 1 176

Bond J. E. Sierwald P. 2002 Cryptic speciation in the Anadenobolus excisus millipede species complex on the island of Jamaica. Evolution 56 1123 1135

Branch W. R. 1982 Hemipeneal morphology of Platynotan lizards. Journal of Herpetology 16 16 38

Bremer K. 1988 The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42 795 803 DOI

Burbrink F. T. Lawson R. Slowinski J. B. 2000 Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54 2107 2118

Card W. Kluge A. G. 1995 Hemipenal skeleton and varanid lizard systematics. Journal of Herpetology 29 275 280

Cogger H. G. (2000). ‘Reptiles and Amphibians of Australia.’ (Reed New Holland: Sydney.)

Comstock K. E. Ostrander E. A. Wasser S. K. 2003 Amplifying nuclear and mitochondrial DNA from African elephant ivory: a tool for monitoring the ivory trade. Conservation Biology 17 1840 1843 DOI

Davison A. Birks J. D. S. Brookes R. C. Braithwaite T. C. Messenger J. E. 2002 On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. Journal of Zoology 257 141 143 DOI

De Lisle H. F. (1996). ‘The Natural History of Monitor Lizards.’ (Krieger Publishing Company: Malabar.)

Donnellan S. C. Hutchinson M. N. Saint K. M. 1999 Molecular evidence for the phylogeny of Australian gekkonoid lizards. Biological Journal of the Linnean Society 67 97 118 DOI

Eriksson T. (1998). ‘AutoDecay version 4.0.’ Program distributed by the author. (Bergius Foundation, Royal Swedish Academy of Sciences: Stockholm.)

Estes R. (1983). ‘Handbuch der Paläoherpetologie. Teil 10A, Sauria terrestria, Amphisbaenia.’ (Gustav Fischer Verlag: Stuttgart.)

Estes R. 1984 Fish, amphibians and reptiles from the Etadunna Formation, Miocene of South Australia. Australian Zoologist 21 335 343

Forstner M. R. J. Davis S. K. Arevalo E. 1995 Support for the hypothesis of anguimorph ancestry for the suborder Serpentes from phylogenetic analysis of mitochondrial sequences. Molecular Phylogenetics and Evolution 4 93 102

Frost D. R. Hillis D. M. 1990 Species in concept and practice: herpetological applications. Herpetologica 46 87 104

Frost D. R. Kluge A. G. 1994 A consideration of epistemology in systematic biology, with special reference to species. Cladistics 10 259 294

Fuller S. Baverstock P. King D. 1998 Biogeographic origins of goannas (Varanidae): a molecular perspective. Molecular Phylogenetics and Evolution 9 294 307 DOI

Giannasi N. Malhotra A. Thorpe R. S. 2001 Nuclear and mtDNA phylogenies of the Trimeresurus complex: implications for the gene versus species tree debate. Molecular Phylogenetics and Evolution 19 57 66 DOI

Hebert P. D. N. Cywinska A. Ball S. L. deWaard J. R. 2003 a Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B. Biological Sciences 270 313 321 DOI

Hebert P. D. N. Ratnasingham S. deWaard J. R. 2003 b Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B. Biological Sciences 270 Suppl. 96 99 DOI

Hecht M. K. 1975 The morphology and relationships of the largest known terrestrial lizard, Megalania prisca Owen, from the Pleistocene of Australia. Proceedings of the Royal Society of Victoria 87 239 250

Hillis D. M. 1998 Taxonomic sampling, phylogenetic accuracy, and investigator bias. Systematic Biology 47 3 8

Hoffstetter R. 1968 Présence des Varanidae (Reptilia: Sauria) dans le Miocène de Catalogne. Considérations sur l’histoire de la famille. Bulletin du Museum Nationale d’Histoire, Naturelle 40 1051 1064

Holmes R. S. King M. King D. 1975 Phenetic relationships among varanid lizards based upon comparative electrophoretic data and karyotypic analyses. Biochemical Systematics and Ecology 3 257 262

Hudson R. R. Turrelli M. 2003 Stochasticity overrules the “three times rule”: genetic drift, genetic draft and coalescent times for nuclear loci versus mitochondrial DNA. Evolution 57 182 190

Huelsenbeck J. P. Ronquist F. 2001 MRBAYES: Bayesian inference of phylogeny. Bioinformatics (Oxford, England) 17 754 755

Huelsenbeck J. P. Hillis D. M. Nielsen R. 1996 A likelihood-ratio test of monophyly. Systematic Biology 45 546 558

Jennings W. B., and Pianka E. R. (2004). Tempo and timing of the Australian Varanus radiation. In ‘Varanoid Lizards of the World’. (Eds E. R. Pianka, D. R. King and R. A. King.) pp. 77–87. (Indiana University Press: Bloomington, IL.)

Jukes T. H., and Cantor C. R. (1969). Evolution of protein molecules. In ‘Mammalian Protein Metabolism’. (Ed. H. N. Munro.) pp. 21–132. (Academic Press: New York.)

Kasper M. L. Reeson A. F. Cooper S. J. B. Perry K. D. Austin A. D. 2004 Assessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA. Molecular Ecology 13 2037 2048

King D., and Green B. (1999). ‘Goannas. The Biology of Varanid Lizards.’ (University of New South Wales Press: Sydney.)

King D. King M. Baverstock P. 1991 A new phylogeny of the Varanidae. Mertensiella 2 211 219

King M. (1990). Chromosomal and immunogenetic data: a new perspective on the origin of Australia’s reptiles. In ‘Cytogenetics of Amphibians and Reptiles. Advances in Life Sciences’. (Ed. E. Olmo.) pp. 153–180. (Birkhauser Verlag: Basel.)

King M. King D. 1975 Chromosomal evolution in the lizard genus Varanus (Reptilia). Australian Journal of Biological Sciences 28 89 108

Lee M. S. Y. 2004 The molecularisation of taxonomy. Invertebrate Systematics 18 1 6

Losos J. B. Greene H. W. 1988 Ecological and evolutionary implications of diet in monitor lizards. Biological Journal of the Linnean Society 35 379 407

Macey J. R. Verma A. 1997 Homology in phylogenetic analysis: alignment of transfer RNA genes and the phylogenetic position of snakes. Molecular Phylogenetics and Evolution 7 272 279

Maddison W. P., and Maddison D. R. (1992). ‘MacClade. Analysis of Phylogeny and Character Evolution.’ (Sinauer: Sunderland, MA.)

Mallet J. Willmott K. 2003 Taxonomy: renaissance or Tower of Babel? Trends in Ecology & Evolution 18 57 59 DOI

Mayr E. 1982 Of what use are subspecies? Auk 99 593 595

McDowell S. B. Bogert C. M. 1954 The systematic position of Lanthanotus and the affinities of the anguinomorphan lizards. Bulletin of the American Museum of Natural History 105 1 142

Molbo D. Machado C. A. Sevenster J. G. Keller L. Herre E. A. 2003 Cryptic species of fig-pollinating wasps: implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation. Proceedings of the Royal Society of London. Series B. Biological Sciences 100 5867 5872

Molnar R. E. (2004). The long and honorable history of monitors and their kin. In ‘Varanoid Lizards of the World’. (Eds E. R. Pianka, D. R. King and R. A. King.) pp. 10–67. (Indiana University Press: Bloomington, IL.)

Momen H. 2002 Molecular taxonomy of trypanosomatids: some problems and pitfalls. Archives of Medical Research 33 413 415

Moore W. S. 1995 Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49 718 726 DOI

Moreira D. Philippe H. 2000 Molecular phylogeny: pitfalls and progress. International Microbiology 3 9 16

Nee S. Holmes E. C. May R. M. Harvey P. H. 1994 Extinction rates can be estimated from molecular phylogenies. Philosophical Transactions of the Royal Society of London Series B 344 77 82

Nelson W. S. Prodöhl P. A. Avise J. C. 1996 Development and application of long-PCR for the assay of full-length animal mitochondrial DNA. Molecular Ecology 5 807 810

Nelson W. S. Dean T. Avise J. C. 2000 Matrilineal history of the endangered Cape Sable seaside sparrow inferred from mitochondrial DNA polymorphism. Molecular Ecology 9 809 813

Noell C. J. Donnellan S. Foster R. Haigh L. 2001 Molecular discrimination of garfish Hyporhamphus (Beloniformes) larvae in southern Australian waters. Marine Biotechnology 3 509 514

Page R. D. M. Charleston M. A. 1997 From gene to organismal phylogeny: reconciled trees and the gene tree/species tree problem. Molecular Phylogenetics and Evolution 7 231 240

Palumbi S., Martin A., Romano S., McMillan W. O., Stice L., and Grabowski G. (1991). ‘The Simple Fool’s Guide to PCR Version 2.’ (Department of Zoology and Kewalo Marine Laboratory, University of Hawaii: Honolulu, HI.)

Pepin D. J. 1999 The origin of monitor lizards based on a review of the fossil evidence. Mertensiella 11 11 42

Pianka E. R., King D. R., and King R. A. (2004). ‘Varanoid Lizards of the World.’ (Indiana University Press: Bloomington, IL.)

Posada D. Crandall K. A. 1998 Modeltest: testing the model of DNA substitution. Bioinformatics 14 817 818

Pregill G. K. Gauthier J. A. Greene H. W. 1986 The evolution of helodermatid squamates, with description of a new taxon and an overview of Varanoidea. Transactions of the San Diego Society of Natural History 21 167 202

Rambaut A. (1995). ‘Se-Al. Sequence Alignment Editor.’ (Evolutionary Biology Unit, University of Oxford: Oxford, UK.) Available at [Verified 10 July 2006].

Rambaut A. Harvey P. H. Nee S. 1997 End-Epi: an application for inferring phylogenetic and population dynamical processes from molecular sequences. Computer Applications in the Biosciences 13 303 306

Reed E. Hutchinson M. N. 2005 First record of a giant varanid (Megalania, Squamata) from the Pleistocene of Naracoorte, South Australia. Memoirs of the Queensland Museum 51 203 213

Rocha-Olivares A. Moser H. G. Stannard J. 2000 Molecular identification and description of pelagic young of the rockfishes Sebastes constellatus and Sebastes ensifer. Fishery Bulletin 98 353 363

Rodriguez F. Oliver J. F. Marín A. Medina J. R. 1990 The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142 485 501

Schluter D. (2000). ‘The Ecology of Adaptive Radiation.’ (Oxford University Press: Oxford.)

Shine R. Harlow P. S. Keogh J. S. Boeadi 1996 Commercial harvesting of giant lizards: the biology of water monitors Varanus salvator in southern Sumatra. Biological Conservation 77 125 134

Shine R. Ambariyanto Harlow P. S. Mumpuni 1998 Ecological traits of commercially harvested water monitors, Varanus salvator, in northern Sumatra. Wildlife Research 25 437 447 DOI

Simmons M. P. Ochoterena H. 2000 Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49 369 381 DOI

Sprackland R. G. 1991 The origin and zoogeography of monitor lizards of the subgenus Odatria GRAY (Sauria: Varanidae): a re-evaluation. Mertensiella 2 240 252

Steel R. (1997). ‘Living Dragons. A Natural History of the World’s Monitor Lizards.’ (RD Press: Sydney.)

Swofford D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*And Other Methods).’ (Sinauer: Sunderland, MA.)

Takeyama H. Tsuzuki H. Chow S. Nakayama H. Matsunaga T. 2000 Discrimination between Atlantic and Pacific subspecies of northern bluefin tuna (Thunnus thynnus) by magnetic-capture hybridization using bacterial magnetic probes. Marine Biotechnology 2 309 313

Tautz D. Arctander P. Minelli A. Thomas R. H. Vogler A. P. 2003 A plea for DNA taxonomy. Trends in Ecology & Evolution 18 70 74

Thalmann O. Hebler J. Poinar H. N. Pääbo S. Vigilant L. 2004 Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Molecular Ecology 13 321 335 DOI

Townsend T. M. Larson A. Louis E. Macey J. R. 2004 Molecular phylogenetics of Squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Systematic Biology 53 735 757 DOI

TRAFFIC International (2003). ‘What are the main wildlife commodities in trade? 25 years of TRAFFIC.’ Available at [Verified August 2003].

Vidal N. Hedges S. B. 2004 Molecular evidence for a terrestrial origin of snakes. Proceedings of the Royal Society of London. Series B. Biological Sciences 271 Suppl. S226 S229

Vincent M., and Wilson S. (1999). ‘Australian Goannas.’ (New Holland Publishers: Sydney.)

Vincent S. Vian J. M. Carlotti M. P. 2000 Partial sequencing of the cytochrome oxydase b subunit gene 1: a tool for the identification of European species of blow flies for postmortem interval estimation. Journal of Forensic Sciences 45 820 823

Welter C. Dooley S. Blin N. 1989 A rapid protocol for the purification of mitochondrial DNA suitable for studying restriction fragment length polymorphisms. Gene 83 169 172

Wetton J. H. Tsang C. S. F. Roney C. A. Spriggs A. C. 2004 An extremely sensitive species-specific ARMs PCR test for the presence of tiger bone DNA. Forensic Science International 140 139 145 DOI

Wilson E. O. Brown W. L. 1953 The subspecies concept and its taxonomic application. Systematic Zoology 2 97 111 DOI

Zhang D.-X. Hewitt G. M. 1996 Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution 11 247 251 DOI

Ziegler T. Böhme W. 1999 Genital morphology and systematics of two recently described monitor lizards of the Varanus (Euprepiosaurus) indicus group. Mertensiella 11 121 128

Ziegler T. Böhme W. Eidenmüller B. Philipp K. M. 2001 A note on the coexistence of three species of Pacific monitor lizards in Australia (Sauria, Varanidae, Varanus indicus group). Bonner Zoologische Beiträge, Bonn 50 27 30

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