Register      Login
Emu Emu Society
Journal of BirdLife Australia
RESEARCH ARTICLE

Molecular resolution of population history, systematics and historical biogeography of the Australian ringneck parrots Barnardius: are we there yet?

Leo Joseph A C and Thomas Wilke B
+ Author Affiliations
- Author Affiliations

A Department of Ornithology, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103-1195, USA. Present address: Australian National Wildlife Collection, CSIRO Sustainable Ecosystems, GPO Box 284, Canberra, ACT 2601, Australia.

B Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32 (IFZ), D-35392 Giessen, Germany.

C Corresponding author. Email: leo.joseph@csiro.au

Emu 106(1) 49-62 https://doi.org/10.1071/MU05035
Submitted: 30 June 2005  Accepted: 22 December 2005   Published: 10 March 2006

Abstract

The Australian Ringneck (Barnardius zonarius) shows clear geographical replacement of populations across its range. These populations have been given taxonomic epithets barnardi, zonarius, semitorquatus and macgillivrayi. We investigated whether historical or non-historical processes explain the origin of their phenotypic differentiation from each other. We used complete ND2 gene sequences from mitochondrial DNA (mtDNA) to test whether there is geographical coincidence of breaks in phenotypic and neutral molecular diversity. Simply, geographical coincidence is expected by historical processes but not by non-historical ones. Phylogenetic analysis identified one clade with most barnardi samples and another with zonarius, semitorquatus and macgillivrayi. The latter included some phenotypically typical barnardi but they were from localities where it approaches zonarius and macgillivrayi. Differentiation between the two clades, and thus of barnardi from all other populations, likely occurred first by a historical process such as vicariance. Later gene flow appears to have eroded the mtDNA monophyly of barnardi. Phenotypic and mtDNA diversity among semitorquatus, zonarius and macgillivrayi are not correlated. Non-historical processes are clearly suggested in the origin of their phenotypic differentiation. Their low nucleotide diversity, however, leaves ambiguity as to whether very recent historical processes could have been involved. Ramifications to issues of Barnardius systematics are discussed. Isolated north-western Queensland populations (macgillivrayi) are not closely related to barnardi. Alternative taxonomic treatments of our findings, recognising no more than three taxa (barnardi, zonarius and macgillivrayi) under different species concepts are cautiously discussed while urging more study.


Acknowledgments

ANSP-based field and laboratory work was funded by the Rodolphe Meyer de Schauensee Fund (ANSP), by kind donations made by LJ’s ANSP colleagues to the Save the Leo Fund (2001) and to a fund in the memory of George and Mary Joseph (2004). It was further aided by National Science Foundation Major Research Instrumentation Grant No. 9871363 to the Laboratory for Molecular Systematics and Evolution at the Academy of Natural Sciences, Philadelphia. For being such a wonderful field crew without whom three major field trips could not have happened LJ wishes to thank W. Boles, A. Nyari, L. Pedler, N. Rice, and J. Wieneke. Samples were collected and exported to ANSP under ethics, scientific collecting and export permits kindly granted by Environment Australia, Wildlife Science and Management Section Canberra (V. Chung, C. Robinson); Queensland Department of Primary Industries’ Animal Ethics Committee (A. Kelly, G. Smith); Queensland Environmental Protection Agency, Queensland Parks and Wildlife Service (M. Nissen); Biodiversity Management Unit, National Parks and Wildlife Service, New South Wales (S. Nand); National Parks and Wildlife Service, Department of Environment and Heritage, South Australia (P. Canty, P. Copley); and Department of Conservation and Land Management, Western Australia (P. Mawson). Curators and collection managers at the following museums also helped make the work possible by providing tissue samples and other support especially relating to success of field trips: South Australian Museum (S. Donnellan, P. Horton, A. Hugall, M. Penck), Australian Museum (W. Boles), Museum Victoria (L. Christidis, J. Norman, N. W. Longmore), Western Australian Museum (R. Johnstone, B. Maryan, R. How), Queensland Museum, (H. Janetzki, S. Van Dyck, B. Done, J. Wieneke). We thank all landowners and managers who kindly allowed us to stay and collect on their properties and for their great hospitality and support, in particular Angus and Karen Emmott (Noonbah), Sandy Morris and family (Yardea), and Mary and Mac Haig (Alroy). A. Baker, J. Bowler, D. Alpers, S. Bellman, D. Cohen and J. Wieneke also supported the work in diverse ways. Dr J. Rozas once again kindly gave of his time to advise on analyses though any faults in the analyses are not his. We sincerely thank three anonymous reviewers for their stern remarks that tightened and, we hope, substantially improved the paper.


References

Alfaro, M. E. , Zoller, S. , and Lutzoni, F. (2003). Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Molecular Biology and Evolution 20, 255–266.
Crossref | GoogleScholarGoogle Scholar | PubMed | Barrett G. , Silcocks A. , Barry S. , Cunningham R. , and Poulter R. (2003). ‘The New Atlas of Australian Birds.’ (RAOU: Melbourne.)

Bowler J. M. (1982). Aridity in the late Tertiary and Quaternary of Australia. In ‘Evolution of the Flora and Fauna of Arid Australia’. (Eds W. R. Barker and P. J. M. Greenslade.) pp. 35–45. (Peacock Publications: Adelaide.)

Cabot, E. L. , and Beckenbach, A. T. (1989). Simultaneous editing of multiple nucleic acid and protein sequences with ESEE. Computer Applications in the Biosciences 5, 233–234.
PubMed | Collar N. (1997). Family Psittacidae (Parrots). In ‘Handbook of the Birds of the World. Vol. 4. Sandgrouse to Cuckoos’. (Eds J. del Hoyo, A. Elliott and J. Sargatal.) pp. 280–477. (Lynx Edicions: Barcelona.)

Condon, H. T. (1941). The Australian broadtailed parrots (subfamily Platycercinae). Records of the South Australian Museum 7, 117–144.
Crome F. , and Shields J. (1992). ‘Parrots and Pigeons of Australia.’ (Angus and Robertson: Sydney.)

David T. W. E. (1950). ‘The Geology of the Commonwealth of Australia.’ (Edward Arnold: London.)

Douady, C. J. , Delsuc, F. , Boucher, Y. , Doolittle, W. F. , and Douzery, E. J. P. (2003). Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Molecular Biology and Evolution 20, 248–254.
Crossref | GoogleScholarGoogle Scholar | PubMed | Fisher C. D. (1970). Geographic variation and evolution in the Australian Ringneck Parrot (Barnardius). Ph.D. Thesis, University of Michigan, Ann Arbor, MI.

Ford, J. (1974). Speciation in Australian birds adapted to arid habitats. Emu 74, 161–168.
Forshaw J. M. , and Cooper W. T. (1981). ‘Australian Parrots.’ 2nd edn. (Landsdowne Editions: Melbourne.)

Forshaw J. M. , and Cooper W. T. (2002). ‘Australian Parrots.’ 3rd edn. (Alexander Editions: Robina, Qld.)

Fu, Y.-X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
PubMed | Higgins P. J. (Ed.) (1999). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 4: Parrots to Dollarbird.’ (Oxford University Press: Melbourne.)

Hill, R. S. (2004). Origins of the southeastern Australian vegetation. Proceedings of the Royal Society of London. Series B. Biological Sciences 359, 1537–1549.
Crossref | GoogleScholarGoogle Scholar | Johnstone R. , and Storr G. M. (1998). ‘Handbook of Western Australian Birds. Vol. 1: Non-Passerines.’ (Western Australian Museum: Perth.)

Joseph, L. , and Wilke, T. (2004). When DNA throws a spanner in the taxonomic works: testing for monophyly in the Dusky-capped Flycatcher Myiarchus tuberculifer and its South American subspecies M. t. atriceps Cabanis, 1883. Emu 104, 197–204.
Crossref | GoogleScholarGoogle Scholar | Juniper T. , and Parr M. (1998). ‘Parrots. A Guide to Parrots of the World.’ (Yale University Press: New Haven, CT.)

Keast, J. A. (1961). Bird speciation on the Australian continent. Bulletin of the Museum of Comparative Zoology 123, 303–495.
Schodde R. (1982). Origin, adaptation and evolution of birds in arid Australia. In ‘Evolution of the Flora and Fauna of Arid Australia’. (Eds W. R. Barker and P. J. M. Greenslade.) pp. 191–224. (Peacock Publications: Adelaide.)

Schodde R. , and Mason I. J. (1997). Aves (Columbidae to Coraciidae). In ‘Zoological Catalogue of Australia. Vol. 37.2’. (Eds W. W. K. Houston and A. Wells.) (CSIRO Publishing: Melbourne.)

Schodde R. , and Mason I. J. (1999). ‘The Directory of Australian Birds: Passerines.’ (CSIRO Publishing: Melbourne.)

Serventy D.L. (1972). Causal ornithogeography of Australia. In ‘Proceedings of the 15th International Ornithological Congress, The Hague’. (Ed. K. Voous.) pp. 574–584. (E. J. Brill: Leiden, The Netherlands.)

Serventy D. L. , and Whittell H. M. (1976). ‘Birds of Western Australia.’ 5th edn. (University of Western Australia Press: Perth.)

Sunnucks, P. (2000). Efficient genetic markers for population biology. Trends in Ecology & Evolution 15, 199–203.
Crossref | GoogleScholarGoogle Scholar | Swofford D. (2002). ‘PAUP 4.0b10. Phylogenetic Analysis Using Parsimony.’ (Sinauer: Sunderland, MA.)

Tajima, F. (1989). The effect of change in population size on DNA polymorphism. Genetics 125, 597–601.
Wheeler Q. , and Meier R. (Eds) (2000). ‘Species Concepts and Phylogenetic Theory. A Debate.’ (Columbia University Press: New York.)

Wiens, J. J. , and Servedio, M. R. (1998). Phylogenetic analysis and intraspecific variation: performance of parsimony, likelihood, and distance methods. Systematic Biology 47, 228–253.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Wooller, R. D. , Saunders, D. A. , Bradley, J. S. , and de Rebeira, C. P. (1985). Geographical variation in size of an Australian honeyeater (Aves : Meliphagidae): an example of Bergmann’s rule. Biological Journal of the Linnean Society 25, 355–363.


Zink, R. M. (2002). A new perspective on the evolutionary history of Darwin’s finches. Auk 119, 864–871.


Zink, R. M. (2005). Natural selection on mitochondrial DNA in Parus and its relevance for phylogeographic studies. Proceedings of the Royal Society of London. Series B. Biological Sciences 272, 71–78.
Crossref | GoogleScholarGoogle Scholar |





Appendix 1.  Details of specimens of Barnardius zonarius and outgroups studied
All specimen numbers are of tissue samples in the collection of the Academy of Natural Sciences, Philadelphia (ANSP). All corresponding voucher skins, most which are in ANSP, the Australian Museum, Sydney, and Kansas University Museum of Natural History, Lawrence, Kansas, can be obtained from the collection databases of those institutions. Note that zE and zW refer to eastern and western samples of zonarius, respectively (see Fig. 1). NSW – New South Wales; Qld – Queensland; SA – South Australia; WA – Western Australia
Click to zoom