Emu Emu Society
Journal of BirdLife Australia
RESEARCH ARTICLE

The impact of Pleistocene changes of climate and landscape on Australian birds: a test using the Pied Butcherbird (Cracticus nigrogularis)

Anna M. Kearns A C , Leo Joseph B and Lyn G. Cook A

A The University of Queensland, School of Biological Sciences, Brisbane, Qld 4072, Australia.

B Australian National Wildlife Collection, CSIRO Ecosystem Sciences, GPO Box 284, Canberra, ACT 2601, Australia.

C Corresponding author. Email: a.kearns@uq.edu.au

Emu 110(4) 285-295 http://dx.doi.org/10.1071/MU10020
Submitted: 22 March 2010  Accepted: 30 June 2010   Published: 26 October 2010

Abstract

Widespread cyclic aridity during the Pleistocene is hypothesised to have had a significant impact on widespread Australian birds causing range-wide contractions to historical refugia and population differentiation while in isolation. In this study we tested a priori hypotheses for the impact of Pleistocene climatic and edaphic changes on the population history of the widespread Australian Pied Butcherbird (Cracticus nigrogularis). Analysis of mitochondrial DNA sequences from 55 individuals of C. nigrogularis revealed low genetic diversity, poor geographical structure and signatures of a recent demographic expansion. In contrast with long-standing biogeographical hypotheses, our data suggest that C. nigrogularis was likely to have been restricted to multiple refugia across its current range rather than undergoing range-wide contractions to one or few refugia. In addition, we found no evidence for the Carpentarian Barrier of northern Australia having limited dispersal in C. nigrogularis, which contrasts with predictions from intraspecific taxonomy and with population structures of several other bird species. Our data add to the increasing number of phylogeographical studies of widespread Australian birds that show evidence of maintaining large effective population sizes despite widespread aridity, as well as species-specific, rather than ecosystem-wide, responses to Pleistocene climatic changes and biogeographical barriers.

Additional keywords: Aves, Carpentarian Gap, Corvoidea, intraspecific divergence, phylogeography, population bottleneck.


References

Amadon, D. (1951). Taxonomic notes on the Australian butcher-birds (family Cracticidae). American Museum Novitates 1504, 1–33. open url image1

Arbogast, B. S., Edwards, S. V., Wakeley, J., Beerli, P., and Slowinski, J. B. (2002). Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annual Review of Ecology Evolution and Systematics 33, 707–740.
Estimating divergence times from molecular data on phylogenetic and population genetic timescales.CrossRef | open url image1

Avise, J. C. (2000). ‘Phylogeography: The History and Formation of a Species.’ (Harvard University Press: Cambridge, MA.)

Avise, J. C., and Walker, D. (1998). Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 457–463.
Pleistocene phylogeographic effects on avian populations and the speciation process.CrossRef | open url image1

Barrett, G., Silcocks, A., Barry, S., Cunningham, R., and Poulter, R. (2003). ‘The New Atlas of Australian Birds.’ (Royal Australian Ornithologists Union: 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.)

Bowler, J. M., Kotsonis, A., and Lawrence, C. R. (2006). Environmental evolution of the mallee region, western Murray Basin. Proceedings of the Royal Society of Victoria 118, 161–210. open url image1

Bowman, D. M. J. S., Brown, G. K., Braby, M. F., Brown, J. R., Cook, L. G., Crisp, M. D., Ford, F., Haberle, S., Hughes, J., Isagi, I., Joseph, L., McBride, J., Nelson, G., and Ladiges, P. Y. (2010). Biogeography of the Australian monsoon tropics. Journal of Biogeography 37, 201–216.
Biogeography of the Australian monsoon tropics.CrossRef | open url image1

Braby, M. (2008). Biogeography of butterflies in the Australian monsoon tropics. Australian Journal of Zoology 56, 41–56.
Biogeography of butterflies in the Australian monsoon tropics.CrossRef | open url image1

Byrne, M., Yeates, D. K., Joseph, L., Bowler, J., Cooper, S., Donnellan, S. C., Kearney, M., Keogh, J. S., Leijs, R., Melville, J., Murphy, D., Porch, N., Williams, M. A., and Wyrwoll, K.-H. (2008). Birth of a biome: synthesizing environmental and molecular studies of the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
Birth of a biome: synthesizing environmental and molecular studies of the assembly and maintenance of the Australian arid zone biota.CrossRef | 18761619PubMed | open url image1

Carstens, B. C., and Knowles, L. (2007). Shifting distributions and speciation: species divergence during rapid climate change. Molecular Ecology 16, 619–627.
Shifting distributions and speciation: species divergence during rapid climate change.CrossRef | 17257117PubMed | open url image1

Carstens, B. C., and Richards, C. L. (2007). Integrating coalescent and ecological niche modeling in comparative phylogeography. Evolution 61, 1439–1454.
Integrating coalescent and ecological niche modeling in comparative phylogeography.CrossRef | 17542851PubMed | open url image1

Castelloe, J., and Templeton, A. R. (1994). Root probabilities for intra-specific gene trees under neutral coalescent theory. Molecular Phylogenetics and Evolution 3, 102–113.
Root probabilities for intra-specific gene trees under neutral coalescent theory.CrossRef | 8075830PubMed | open url image1

Chapple, D. G., and Keogh, J. S. (2004). Parallel adaptive radiations in arid and temperate Australia: molecular phylogeography and systematics of the Egernia whitii (Lacertilia:Scincidae) species group. Biological Journal of the Linnean Society 83, 157–173.
Parallel adaptive radiations in arid and temperate Australia: molecular phylogeography and systematics of the Egernia whitii (Lacertilia:Scincidae) species group.CrossRef | open url image1

Chivas, A. R., Garcia, A., and van der Kaars, S. (2001). Sea-level and environmental changes since the last interglacial in the Gulf of Carpentaria, Australia: an overview. Quaternary International 83–85, 19–46.
Sea-level and environmental changes since the last interglacial in the Gulf of Carpentaria, Australia: an overview.CrossRef | open url image1

Clement, M., Posada, D., and Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS: a computer program to estimate gene genealogies.CrossRef | 11050560PubMed | open url image1

Cracraft, J. (1986). Origin and evolution of continental biotas, speciation and historical congruence within the Australian avifauna. Evolution 40, 977–996.
Origin and evolution of continental biotas, speciation and historical congruence within the Australian avifauna.CrossRef | open url image1

Cracraft, J. (1991). Patterns of diversification within continental biotas, hierarchical congruence among the areas of endemism of Australian vertebrates. Australian Systematic Botany 4, 211–227.
Patterns of diversification within continental biotas, hierarchical congruence among the areas of endemism of Australian vertebrates.CrossRef | open url image1

Crisp, M. D., and Cook, L. G. (2007). A congruent molecular signature of vicariance across multiple plant lineages. Molecular Phylogenetics and Evolution 43, 1106–1117.
A congruent molecular signature of vicariance across multiple plant lineages.CrossRef | 17434758PubMed | open url image1

Edwards, S. V. (1993). Long-distance gene flow in a cooperative breeder detected in genealogies of mitochondrial DNA sequences. Proceedings of the Royal Society of London. Series B. Biological Sciences 252, 177–185.
Long-distance gene flow in a cooperative breeder detected in genealogies of mitochondrial DNA sequences.CrossRef | open url image1

Edwards, S. V., and Beerli, P. (2000). Perspective: gene divergence, population divergence, and the variance in the coalescence time in phylogeographic studies. Evolution 54, 1839–1854.
| 11209764PubMed | open url image1

Ford, J. (1974). Speciation in Australian birds adapted to arid habitats. Emu 74, 161–168.
Speciation in Australian birds adapted to arid habitats.CrossRef | open url image1

Ford, J. (1978). Subspeciation in the White-throated Warbler of Australia and New Guinea. Emu 78, 90–92.
Subspeciation in the White-throated Warbler of Australia and New Guinea.CrossRef | open url image1

Ford, J. (1987). Hybrid zones in Australian birds. Emu 87, 158–178.
Hybrid zones in Australian birds.CrossRef | open url image1

Ford, F., and Blair, D. (2005). Neat patterns with a messy history: savannah refuges in northern Australia. Mammal Study 30, S45–S50.
Neat patterns with a messy history: savannah refuges in northern Australia.CrossRef | open url image1

Fu, Y.-X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.
| 9335623PubMed | open url image1

Fu, Y.-X., and Li, W. H. (1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709.
| 8454210PubMed | open url image1

Hackett, S. J. (1996). Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Molecular Phylogenetics and Evolution 5, 368–382.
Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves).CrossRef | 8728395PubMed | open url image1

Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 359, 183–195.
Genetic consequences of climatic oscillations in the Quaternary.CrossRef | open url image1

Higgins, P. J., Peter, J. M., and Cowling, S. J. (Eds) (2006). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 7: Boatbill to Starlings.’ (Oxford University Press: Melbourne.)

Ho, S. Y. M. (2007). Calibrating molecular estimates of substitution rates and divergence times in birds. Journal of Avian Biology 38, 409–414. open url image1

Ho, S. Y. W., Phillips, M. J., Cooper, A., and Drummond, A. J. (2005). Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution 22, 1561–1568.
Time dependency of molecular rate estimates and systematic overestimation of recent divergence times.CrossRef | 15814826PubMed | open url image1

Hudson, R. R. (2000). A new statistic for detecting genetic differentiation. Genetics 155, 2011–2014.
| 10924493PubMed | open url image1

Jennings, W. B., and Edwards, S. V. (2005). Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees. Evolution 59, 2033–2047.
| 16261740PubMed | open url image1

Johnson, N. K., and Cicero, C. (2004). New mitochondrial DNA data affirm the importance of Pleistocene speciation in North American birds. Evolution 58, 1122–1130.
| 15212392PubMed | open url image1

Joseph, L. (2008). The changing faces of systematics and biogeography in Australian ornithology in the latter half of the twentieth century: a young turk’s view. In ‘Contributions to the History of Australasian Ornithology. Memoirs of the Nuttall Ornithological Club 14’. (Eds W. E. Davis Jr, H. F. Recher, W. E. Boles and J. A. Jackson.) pp. 253–304. (Nuttall Ornithological Club: Cambridge, MA.)

Joseph, L., and Omland, K. E. (2009). Phylogeography: its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds. Emu 109, 1–23.
Phylogeography: its development and impact in Australo-Papuan ornithology with special reference to paraphyly in Australian birds.CrossRef | open url image1

Joseph, L., and Wilke, T. (2006). Molecular resolution of population history, systematics and historical biogeography of the Australian ringneck parrots Barnardius: are we there yet? Emu 106, 49–62.
Molecular resolution of population history, systematics and historical biogeography of the Australian ringneck parrots Barnardius: are we there yet?CrossRef | open url image1

Joseph, L., and Wilke, T. (2007). Lack of phylogeographical structure in three widespread Australian birds reinforces emerging challenges in Australian historical biogeography. Journal of Biogeography 34, 612–624.
Lack of phylogeographical structure in three widespread Australian birds reinforces emerging challenges in Australian historical biogeography.CrossRef | open url image1

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.
Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield’s Bronze-Cuckoo Chalcites basalis of Australia.CrossRef | 11972768PubMed | open url image1

Joseph, L., Wilke, T., Ten Have, J., and Chesser, R. T. (2006). 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 37, 625–636.
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.CrossRef | open url image1

Joseph, L., Adcock, G. J., Linde, C., Omland, K. E., Heinsohn, R., Chesser, R. T., and Roshier, D. (2009). A tangled tale of two teal: population history of the Grey Anas gracilis and Chestnut Teal A. castanea of Australia. Journal of Avian Biology 40, 430–439.
A tangled tale of two teal: population history of the Grey Anas gracilis and Chestnut Teal A. castanea of Australia.CrossRef | open url image1

Kearns, A. M., Joseph, L., Edwards, S. V., and Double, M. C. (2009). Inferring the phylogeography and evolutionary history of the Splendid Fairy-wren Malurus splendens from mitochondrial DNA and spectrophotometry. Journal of Avian Biology 40, 7–17.
Inferring the phylogeography and evolutionary history of the Splendid Fairy-wren Malurus splendens from mitochondrial DNA and spectrophotometry.CrossRef | open url image1

Keast, J. A. (1961). Bird speciation on the Australian continent. Bulletin of the Museum of Comparative Zoology 123, 303–495. open url image1

Kirchman, J. J., Hackett, S. J., Goodman, S. M., and Bates, J. M. (2001). Phylogeny and systematics of ground rollers (Brachypteraciidae) of Madagascar. Auk 118, 849–863.
Phylogeny and systematics of ground rollers (Brachypteraciidae) of Madagascar.CrossRef | open url image1

Klicka, J., and Zink, R. M. (1999). Pleistocene effects on North American songbird evolution. Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 695–700.
Pleistocene effects on North American songbird evolution.CrossRef | open url image1

Kuch, U., Keogh, J. S., Weigel, J., Smith, L. A., and Mebs, D. (2005). Phylogeography of Australia’s king brown snake (Pseudechis australis) reveals Pliocene divergence and Pleistocene dispersal of a top predator. Naturwissenschaften 92, 121–127.
Phylogeography of Australia’s king brown snake (Pseudechis australis) reveals Pliocene divergence and Pleistocene dispersal of a top predator.CrossRef | 15688185PubMed | open url image1

Lee, J. Y., and Edwards, S. V. (2008). Divergence across Australia’s Carpentarian Barrier: statistical phylogeography of the Red-backed Fairywren (Malurus melanocephalus). Evolution 62, 3117–3134.
Divergence across Australia’s Carpentarian Barrier: statistical phylogeography of the Red-backed Fairywren (Malurus melanocephalus).CrossRef | 19087188PubMed | open url image1

Lorenzen, E. D., Masembe, C., Arctander, P., and Siegismund, H. R. (2010). A long-standing Pleistocene refugium in southern Africa and a mosaic of refugia in East Africa: insights from mtDNA and the common eland antelope. Journal of Biogeography 37, 571–581.
A long-standing Pleistocene refugium in southern Africa and a mosaic of refugia in East Africa: insights from mtDNA and the common eland antelope.CrossRef | open url image1

Lovette, I. (2004). Mitochondrial dating and mixed support for the ‘2%’ rule in birds. Auk 121, 1–6.
Mitochondrial dating and mixed support for the ‘2%’ rule in birds.CrossRef | open url image1

MacDonald, J. D. (1969). Notes on the taxonomy of Neositta. Emu 69, 169–174.
Notes on the taxonomy of Neositta.CrossRef | open url image1

Markgraf, V., McGlone, M., and Hope, G. (1995). Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective. Trends in Ecology & Evolution 10, 143–147.
Neogene paleoenvironmental and paleoclimatic change in southern temperate ecosystems – a southern perspective.CrossRef | open url image1

Milá, B., Girman, D. J., Kimura, M., and Smith, T. B. (2000). Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird. Proceedings of the Royal Society of London. Series B. Biological Sciences 267, 1033–1040.
Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird.CrossRef | open url image1

Milá, B., McCormack, J. E., Castaneda, G., Wayne, R. K., and Smith, T. B. (2007). Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco. Proceedings of the Royal Society of London. Series B. Biological Sciences 274, 2653–2660.
Recent postglacial range expansion drives the rapid diversification of a songbird lineage in the genus Junco.CrossRef | open url image1

Morgan, M. J., Roberts, J. D., and Keogh, J. S. (2007). Molecular phylogenetic dating supports an ancient endemic speciation model in Australia’s biodiversity hotspot. Molecular Phylogenetics and Evolution 44, 371–385.
Molecular phylogenetic dating supports an ancient endemic speciation model in Australia’s biodiversity hotspot.CrossRef | 17275343PubMed | open url image1

Neaves, L., Zenger, K., Prince, R. T., Eldreidge, B., and Cooper, D. W. (2009). Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus. Molecular Ecology 18, 3363–3378.
Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus.CrossRef | 19659477PubMed | open url image1

Nicholls, J. A., Double, M. C., Rowell, D. M., and Magrath, R. D. (2000). The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). Journal of Avian Biology 31, 165–176.
The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae).CrossRef | open url image1

Omland, K. E., Baker, J. M., and Peters, J. L. (2006). Genetic signatures of intermediate divergence: population history of old and new world holarctic Ravens (Corvus corax). Molecular Ecology 15, 795–808.
Genetic signatures of intermediate divergence: population history of old and new world holarctic Ravens (Corvus corax).CrossRef | 16499703PubMed | open url image1

Peakall, R., and Smouse, P. E. (2001). ‘GENALEX Version 5: Genetic Analyses in Excel. Population Genetic Software for Teaching and Research.’ (Australian National University: Canberra.) Available at http://www.anu.edu.au/BoZo/GenAlEx/ [verified 21 September 2010].

Peterson, A. T., and Nyari, A. S. (2007). Ecological niche conservatism and Pleistocene refugia in the thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62, 173–183.
| 18005155PubMed | open url image1

Qu, Y., Lei, F., Zhang, R., and Lu, X. (2010). Comparative phylogeography of five avian species: implications for Pleistocene evolutionary history in the Qinghai–Tibetan plateau. Molecular Ecology 19, 338–351.
Comparative phylogeography of five avian species: implications for Pleistocene evolutionary history in the Qinghai–Tibetan plateau.CrossRef | 20002586PubMed | open url image1

Ramos-Onsin, S., and Rozas, J. (2002). Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.
| 12446801PubMed | open url image1

Richards, C. L., Carstens, B. C., and Knowles, L. (2007). Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses. Journal of Biogeography 34, 1833–1845.
Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses.CrossRef | open url image1

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.
| 1316531PubMed | open url image1

Rozas, J., Sanchez-DelBanco, J. C., Messequer, X., and Rozas, R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics (Oxford, England) 19, 2496–2497.
DnaSP, DNA polymorphism analyses by the coalescent and other methods.CrossRef | 14668244PubMed | open url image1

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. (2006). Australasia’s bird fauna today – origins and evolutionary development. In ‘Evolution and Biogeography of Australasian Vertebrates’. (Eds J. R. Merrick, M. Archer, G. M. Hickey and M. S. Y. Lee.) pp. 413–458. (Australian Scientific Publishing: Oatlands, NSW.)

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

Swofford, D. L. (2002). ‘PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods).’ v. 4.0b10. (Sinauer: Sunderland, MA.)

Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.
| 2513255PubMed | open url image1

Toon, A., Mather, P. B., Baker, A. M., Durrant, K. L., and Hughes, J. M. (2007). Pleistocene refugia in an arid landscape: analysis of a widely distributed Australian passerine. Molecular Ecology 16, 2525–2541.
Pleistocene refugia in an arid landscape: analysis of a widely distributed Australian passerine.CrossRef | 17561911PubMed | open url image1

Toon, A., Hughes, J., and Joseph, L. (2010). Multilocus analysis of honeyeaters (Aves : Meliphagidae) highlights the spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone. Molecular Ecology , .
Multilocus analysis of honeyeaters (Aves : Meliphagidae) highlights the spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone.CrossRef | 20609078PubMed | open url image1

Weir, J. T., and Schluter, D. (2004). Ice sheets promote speciation in boreal birds. Proceedings of the Royal Society of London. Series B. Biological Sciences 271, 1881–1887.
Ice sheets promote speciation in boreal birds.CrossRef | open url image1

Williams, M. A. J. (2001). Morphoclimatic maps at 18ka, 9ka, & 0ka. In ‘Atlas of Billion-Year Earth History of Australia and Neighbours in Gondwanaland’. (Ed. J. J. Veevers.) pp. 45–48. (GEMOC Press: Sydney.)

Williams, M., Dunkerley, D., De Deckker, P., Kershaw, P., and Chappell, J. (1998). ‘Quaternary Environments.’ 2nd edn. (Arnold: London.)

Williams, M., Cook, E., van der Kaars, S., Barrows, T., Shulmeister, J., and Kershaw, P. (2009). Glacial and deglacial climatic patterns in Australia and surrounding regions from 35 000 to 10 000 years ago reconstructed from terrestrial and near-shore proxy data. Quaternary Science Reviews 28, 2398–2419.
Glacial and deglacial climatic patterns in Australia and surrounding regions from 35 000 to 10 000 years ago reconstructed from terrestrial and near-shore proxy data.CrossRef | open url image1


Export Citation Cited By (20)