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

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: alison.fitch@flinders.edu.au

Australian Journal of Zoology 54(4) 253-269 https://doi.org/10.1071/ZO05038
Submitted: 11 July 2005  Accepted: 9 May 2006   Published: 11 August 2006

Abstract

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.


Acknowledgments

We thank G. Armstrong, J. Armstrong, M. Bonnett, P. Canty, A. de Chambrier, T. Chesser, R. Foster, C. Grant, D. Holland, P. Horner, R. How, M. Hutchinson, R. Leys, B. Maryan, T. Reardon, S. Richards, R. Sadlier, A. Skinner, S. Smith and S. Sweet for kindly collecting and/or donating tissues. Additionally, we thank A. Skinner and two anonymous referees for comments on the manuscript. This work was funded in part by a South Australian Department for Environment and Heritage Wildlife Conservation Fund grant and the Flinders University. AJF was supported by a Flinders University Research award.


References

Arévalo, E. , Davis, S. K. , and Sites, J. (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.
CrossRef |

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

Banks, M. A. , Hedgecock, D. , and 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.
PubMed |

Barraclough, T. G. , and Nee, S. (2001). Phylogenetics and speciation. Trends in Ecology & Evolution 16, 391–399.
CrossRef |

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

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

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. , and 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. , and 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.
CrossRef | PubMed |

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


Bond, J. E. , and Sierwald, P. (2002). Cryptic speciation in the Anadenobolus excisus millipede species complex on the island of Jamaica. Evolution 56, 1123–1135.
CrossRef | PubMed |

Branch, W. R. (1982). Hemipeneal morphology of Platynotan lizards. Journal of Herpetology 16, 16–38.
CrossRef |

Bremer, K. (1988). The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42, 795–803.
CrossRef |

Burbrink, F. T. , Lawson, R. , and 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.
CrossRef | PubMed |

Card, W. , and Kluge, A. G. (1995). Hemipenal skeleton and varanid lizard systematics. Journal of Herpetology 29, 275–280.
CrossRef |

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

Comstock, K. E. , Ostrander, E. A. , and 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.
CrossRef |

Davison, A. , Birks, J. D. S. , Brookes, R. C. , Braithwaite, T. C. , and 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.
CrossRef |

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

Donnellan, S. C. , Hutchinson, M. N. , and Saint, K. M. (1999). Molecular evidence for the phylogeny of Australian gekkonoid lizards. Biological Journal of the Linnean Society 67, 97–118.
CrossRef |

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. , and 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.
CrossRef | PubMed |

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


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

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

Giannasi, N. , Malhotra, A. , and 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.
CrossRef | PubMed |

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

Hebert, P. D. N. , Ratnasingham, S. , and deWaard, J. R. (2003b). 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.
CrossRef |

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.
CrossRef | PubMed |

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. , and King, D. (1975). Phenetic relationships among varanid lizards based upon comparative electrophoretic data and karyotypic analyses. Biochemical Systematics and Ecology 3, 257–262.
CrossRef |

Hudson, R. R. , and 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.
CrossRef | PubMed |

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

Huelsenbeck, J. P. , Hillis, D. M. , and Nielsen, R. (1996). A likelihood-ratio test of monophyly. Systematic Biology 45, 546–558.
CrossRef |

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. , and 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.
CrossRef | PubMed |

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

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

Lee, M. S. Y. (2004). The molecularisation of taxonomy. Invertebrate Systematics 18, 1–6.
CrossRef |

Losos, J. B. , and 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. , and 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.
CrossRef | PubMed |

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

Mallet, J. , and Willmott, K. (2003). Taxonomy: renaissance or Tower of Babel? Trends in Ecology & Evolution 18, 57–59.
CrossRef |

Mayr, E. (1982). Of what use are subspecies? Auk 99, 593–595.


McDowell, S. B. , and 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. , and 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.
CrossRef | PubMed |

Moore, W. S. (1995). Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49, 718–726.
CrossRef |

Moreira, D. , and Philippe, H. (2000). Molecular phylogeny: pitfalls and progress. International Microbiology 3, 9–16.
PubMed |

Nee, S. , Holmes, E. C. , May, R. M. , and 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.
PubMed |

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

Nelson, W. S. , Dean, T. , and Avise, J. C. (2000). Matrilineal history of the endangered Cape Sable seaside sparrow inferred from mitochondrial DNA polymorphism. Molecular Ecology 9, 809–813.
CrossRef | PubMed |

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

Page, R. D. M. , and 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.
CrossRef | PubMed |

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. , and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
CrossRef | PubMed |

Pregill, G. K. , Gauthier, J. A. , and 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 http://evolve.zoo.ox.ac.uk/software.html?id=seal [Verified 10 July 2006].

Rambaut, A. , Harvey, P. H. , and 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.
PubMed |

Reed, E. , and 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. , and 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. , and Medina, J. R. (1990). The general stochastic model of nucleotide substitutions. Journal of Theoretical Biology 142, 485–501.
PubMed |

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

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

Shine, R. , Ambariyanto, , Harlow, P. S. , and Mumpuni, (1998). Ecological traits of commercially harvested water monitors, Varanus salvator, in northern Sumatra. Wildlife Research 25, 437–447.
CrossRef |

Simmons, M. P. , and Ochoterena, H. (2000). Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
CrossRef | PubMed |

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. , and 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.
PubMed |

Tautz, D. , Arctander, P. , Minelli, A. , Thomas, R. H. , and Vogler, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology & Evolution 18, 70–74.
CrossRef |

Thalmann, O. , Hebler, J. , Poinar, H. N. , Pääbo, S. , and 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.
CrossRef | PubMed |

Townsend, T. M. , Larson, A. , Louis, E. , and 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.
CrossRef | PubMed |

TRAFFIC International (2003). ‘What are the main wildlife commodities in trade? 25 years of TRAFFIC.’ Available at http://www.traffic.org/25/wild4_4.htm [Verified August 2003].

Vidal, N. , and 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. , and 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.
PubMed |

Welter, C. , Dooley, S. , and Blin, N. (1989). A rapid protocol for the purification of mitochondrial DNA suitable for studying restriction fragment length polymorphisms. Gene 83, 169–172.
CrossRef | PubMed |

Wetton, J. H. , Tsang, C. S. F. , Roney, C. A. , and 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.
CrossRef | PubMed |

Wilson, E. O. , and Brown, W. L. (1953). The subspecies concept and its taxonomic application. Systematic Zoology 2, 97–111.
CrossRef |

Zhang, D.-X. , and Hewitt, G. M. (1996). Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution 11, 247–251.
CrossRef |

Ziegler, T. , and 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. , and 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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