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

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 | PubMed |

Baker, M. C. (2000). Cultural diversification in the flight call of the Ringneck Parrot in Western Australia. Condor 102, 905–910.


Ballard, J. W. O. , and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.
CrossRef | 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 |

Cain, A. J. (1955). A revision of Trichoglossus haematodus and of the Australian platycercine parrots. Ibis 97, 432–479.


Clement, M. , Posada, D. , and Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1660.
CrossRef | PubMed |

Cracraft, J. (1986). Origin and evolution of continental biotas: speciation and historical congruence within the Australian avifauna. Evolution 40, 977–996.


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.


Crisp, M. D. , Laffan, S. , Linder, H. P. , and Monro, A. (2001). Endemism in the Australian flora. Journal of Biogeography 28, 183–198.
CrossRef |

Crisp, M. D. , Cook, L. , and Steane, D. (2004). Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities. Philosophical Transactions of the Royal Society of London 359, 1551–1771.
CrossRef | PubMed |

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 | PubMed |

Driskell, A. C. , Pruett-Jones, S. , Tarvin, K. A. , and Hagevik, S. (2002). Evolutionary relationships among blue- and black-plumaged populations of the white-winged fairy-wren (Malurus leucopterus). Emu 102, 581–595.


Dulhunty, J. A. (1983). Lake Dieri and its Pleistocene environment of sedimentation, South Australia. Journal and Proceedings of the Royal Society of New South Wales 116, 11–15.


Edwards, S. V. , and Beerli, P. (2000). Perspective: gene divergence, populaton divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54, 1839–1854.
PubMed |

Edwards, S. V. , and Wilson, A. C. (1990). Phylogenetically informative length polymorphism and sequence variability in mitochondrial DNA of Australian babblers (Pomatostomus). Genetics 126, 695–711.
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.


Ford, J. (1987a). Hybrid zones in Australian birds. Emu 87, 158–178.


Ford, J. (1987b). Minor isolates and minor geographical barriers in avian speciation in continental Australia. Emu 87, 90–102.


Ford, J. , and Parker, S. A. (1973). A second species of wedgebill? Emu 73, 113–118.


Ford, J. , and Parker, S. A. (1974). Distribution and taxonomy of some birds from south-western Queensland. Emu 74, 177–194.


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 |

Funk, D. J. , and Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences with insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics 34, 397–423.
CrossRef |

Hawkins, B. A. , Diniz-Filho, J. A. F. , and Soeller, S. A. (2005). Water links the historical and contemporary components of the Australian bird diversity gradient. Journal of Biogeography 32, 1035–1042.
CrossRef |

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 |

Hillis, D. M. , and Huelsenbeck, J. P. (1992). Signal, noise, and reliability in molecular phylogenetic analyses. Journal of Heredity 83, 189–195.
PubMed |

Huelsenbeck, J. P. (1995). Performance of phylogenetic methods in simulation. Systematic Biology 44, 17–48.


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

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 |

Joseph, L. , Wilke, T. , and Alpers, D. (2002). Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield’s Bronze-Cuckoo Chalcites basalis of Australia. Molecular Ecology 11, 829–837.
CrossRef | PubMed |

Joseph, L. , Wilke, T. , Ten Have, J. , and Chesser, R. T. (in press). Implications of mitochondrial DNA polyphyly in two ecologically undifferentiated but morphologically distinct migratory birds, the Masked and White-browed Woodswallows Artamus spp. of inland Australia. Journal of Avian Biology ,


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.


Kinghorn, J. R. (1929). Barnardius occidentalis North and its allies. Emu 29, 1–4.


Kluge, A. (1967). Systematics, phylogeny, and zoogeography of the lizard genus Diplodactylus Gray (Gekkonidae). Australian Journal of Zoology 15, 1007–1108.
CrossRef |

Kolaczkowski, B. , and Thornton, J. W. (2004). Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431, 980–984.
CrossRef | PubMed |

Loffler, E. , and Sullivan, M. E. (1979). Lake Dieri resurrected: an interpretation using satellite imagery. Zeitschrift fur Geomorphologie 23, 233–242.


Lovette, I. (2004). Mitochondrial dating and mixed support for the ‘2% rule’ in birds. Auk 121, 1–6.


McDonald, J. H. , and Kreitman, M. (1991). Adaptive protein evolution at the Adh locus in Drosophila.  Nature 351, 652–654.
CrossRef | PubMed |

Petren, K. , Grant, P. , Grant, B. R. , and Keller, F. (2005). Comparative landscape genetics and the adaptive radiation of Darwin’s finches: the role of peripheral isolation. Molecular Ecology 14, 2943–2957.
CrossRef | PubMed |

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

Posada, D. , and Crandall, K. A. (2001). Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology & Evolution 16, 37–45.
CrossRef |

Rambaut, A. , and Grassly, N. C. (1997). Seq-Gen: An application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees, Version 1.1. Computer Applications in the Biosciences 13, 235–238.
PubMed |

Ramos-Onsin, S. , and Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.
PubMed |

Remsen, J. V. (2005). Pattern, process, and rigor meet classification. Auk 122, 403–413.


Rogers, A. R. , and Harpending, H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.
PubMed |

Rozas, J. , Sánchez-DelBanco, J. C. , Messequer, X. , and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.
CrossRef | PubMed |

Rosenberg, N. A. , and Nordborg, M. (2002). Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nature Reviews. Genetics 3, 380–390.
CrossRef | PubMed |

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 |

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 | 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 |





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
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