A plethora of planigales: genetic variability and cryptic species in a genus of dasyurid marsupials from northern Australia
Michael Westerman A F , Mark J. Blacket B , Ashley Hintz C , Kyle Armstrong D E , Patricia A. Woolley A and Carey Krajewski CA Department of Ecology, Environment and Evolution, La Trobe University, Melbourne, Vic. 3086, Australia.
B Department of Economic Development, Jobs, Transport and Resources, Victoria – AgriBio, 5 Ring Road, Bundoora, Vic. 3083, Australia.
C Department of Zoology, Southern Illinois University, Carbondale, IL 62901, USA.
D Australian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia.
E South Australian Museum, Adelaide, SA 5000, Australia.
F Corresponding author. Email: m.westerman@latrobe.edu.au
Australian Journal of Zoology 64(5) 303-311 https://doi.org/10.1071/ZO16052
Submitted: 28 July 2016 Accepted: 1 December 2016 Published: 22 December 2016
Abstract
Multiple mitochondrial and nuclear gene sequences reveal substantial genetic variation within the dasyurid marsupial genus Planigale, suggesting greater taxonomic diversity than is currently recognised. To further investigate planigale relationships 116 new mitochondrial and nuclear gene sequences, including 16 new specimens, were added to our database. We confirm the presence of an unrecognised species (Planigale ‘species 1’) limited to the Pilbara region of Western Australia and suggest that the ‘Mt Tom Price’ animals may be closely related to Planigale ingrami subtilissima. We also confirm that at least four distinct genetic lineages make up what is currently recognised as P. maculata. This complex of closely related taxa represents a radiation of sibling species rather than a single, genetically diverse one. Three of these lineages (M1 + M2, M3 and M4) are distributed sympatrically across the Top End of Australia and one (M5 = P. maculata sensu stricto) is localised to the eastern coast of Australia. Within the Planigale ingrami complex, Planigale ‘Mt Tom Price’ (lineage Ing. 1) occurs in the Pilbara in sympatry with Planigale ‘species 1’ and lineage Ing. 2 is found in the Northern Territory in sympatry with species of the P. maculata complex. There is thus a plethora of northern Australian planigales, many of which are formally undescribed and whose geographic ranges require careful re-evaluation.
Additional keywords: biogeography, Dasyuridae, phylogenetics, Planigalini, Sminthopsinae, systematics.
References
Aitken, P. (1972). Planigale gilesi (Marsupialia, Dasyuridae); a new species from the interior of south eastern Australia. Records of the South Australian Museum 16, 1–14.Archer, M. (1976). Revision of the marsupial genus Planigale Troughton (Dasyuridae). Memoirs of the Queensland Museum 17, 341–365.
Baverstock, P. R., Archer, M., Adams, M., and Richardson, B. J. (1982). Genetic relationships among 32 species of Australian dasyurid marsupials. In ‘Carnivorous Marsupials’. (Ed. M. Archer.) pp. 641–650. (Royal Zoological Society New South Wales: Sydney.)
Baverstock, P. R., Krieg, M, and Birrell, J (1990). Evolutionary relationships of Australian marsupials as assessed by albumin immunology. Australian Journal of Zoology 37, 273–287.
| Evolutionary relationships of Australian marsupials as assessed by albumin immunology.Crossref | GoogleScholarGoogle Scholar |
Blacket, M., Adams, M., Krajewski, C., and Westerman, M. (2000). Genetic variation within the dasyurid marsupial genus Planigale. Australian Journal of Zoology 48, 443–459.
| Genetic variation within the dasyurid marsupial genus Planigale.Crossref | GoogleScholarGoogle Scholar |
Blacket, M., Kemper, C., and Brandle, R. (2008). Planigales (Marsupialia: Dasyuridae) of eastern Australia’s interior: a comparison of morphology, distributions and habitat preferences, with particular emphasis on South Australia. Australian Journal of Zoology 56, 195–205.
| Planigales (Marsupialia: Dasyuridae) of eastern Australia’s interior: a comparison of morphology, distributions and habitat preferences, with particular emphasis on South Australia.Crossref | GoogleScholarGoogle Scholar |
Burbidge, A. A., Eldridge, M. D. B., Groves, C., Harrison, P. L., Jackson, S. M., Reardon, T. B., Westerman, M., and Woinarski, J. C. Z. (2014). A list of native Australian mammal species and subspecies. In ‘The Action Plan for Australian Mammals 2012’. (Eds J. C. Z. Woinarski, A. A. Burbidge and P. L. Harrison.) pp. 15–32. (CSIRO Publishing: Melbourne.)
Byrne, M., Yeates, D., Joseph, L., Kearney, M., Bowler, J., Williams, M., Cooper, S., Donnellan, S., Keogh, J. S., Leys, R., Melville, J., Murphy, D., Porch, N., and Wyrwoll, K.-H. (2008). Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17, 4398–4417.
| Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjhvFGruw%3D%3D&md5=bd0e826ff070672a007944a97af4d62aCAS |
Catullo, R. A., Lanfear, R., Doughty, P., and Keogh, J. S. (2014). The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae). Journal of Biogeography 41, 659–672.
| The biogeographical boundaries of northern Australia: evidence from ecological niche models and a multi-locus phylogeny of Uperoleia toadlets (Anura: Myobatrachidae).Crossref | GoogleScholarGoogle Scholar |
Drummond, A., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
| BEAST: Bayesian evolutionary analysis by sampling trees.Crossref | GoogleScholarGoogle Scholar |
Drummond, A., Ho, S. Y. W., Phillips, M. J., and Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.
| Relaxed phylogenetics and dating with confidence.Crossref | GoogleScholarGoogle Scholar |
Eldridge, M. D. B., Potter, S., Johnson, C. N., and Ritchie, E. G. (2014). Differing impact of a major biogeographic barrier on genetic structure in two large kangaroos from the monsoon tropics of northern Australia. Ecology and Evolution 4, 554–567.
| Differing impact of a major biogeographic barrier on genetic structure in two large kangaroos from the monsoon tropics of northern Australia.Crossref | GoogleScholarGoogle Scholar |
Gatesy, J., and Springer, M. S. (2014). Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum. Molecular Phylogenetics and Evolution 80, 231–266.
| Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum.Crossref | GoogleScholarGoogle Scholar |
Gould, J. (1851). Description of two new species of Mammalia of the genus Antechinus. Proceedings of the Zoological Society of London 19, 284–285.
| Description of two new species of Mammalia of the genus Antechinus.Crossref | GoogleScholarGoogle Scholar |
Kolaczkowski, B., and Thornton, J. W. (2006). Is there a star tree paradox? Molecular Biology and Evolution 23, 1819–1823.
| Is there a star tree paradox?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVWgs73N&md5=732defebfedfb5a1a799ccb7bb8e8c8dCAS |
Krajewski, C, Blacket, M, Buckley, L, and Westerman, M (1997). A multigene assessment of phylogenetic relationships in the dasyurid marsupial subfamily Sminthopsinae. Molecular Phylogenetics and Evolution 8, 236–248.
| 1:CAS:528:DyaK2sXmsVamu7o%3D&md5=fd8023d963477cd984caba5adc3e2ae4CAS |
Krajewski, C., Wroe, S., and Westerman, M. (2000). Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials. Zoological Journal of the Linnean Society 130, 375–404.
| Molecular evidence for the pattern and timing of cladogenesis in dasyurid marsupials.Crossref | GoogleScholarGoogle Scholar |
Krajewski, C., Anderson, F. E., Woolley, P. A., and Westerman, M. (2012). Molecular evidence for a deep clade of dunnarts (Marsupialia: Dasyuridae: Sminthopsis). Journal of Mammalian Evolution 19, 265–276.
| Molecular evidence for a deep clade of dunnarts (Marsupialia: Dasyuridae: Sminthopsis).Crossref | GoogleScholarGoogle Scholar |
Lönnberg, E. (1913). Results of Dr E. Mjöberg’s Swedish scientific expeditions to Australia 1910–1913. I. Mammals. Kungl. Svenska Vetenskapsakademiens Handlingar 52, 1–10.
Marin, J., Donnellan, S. C., Hedges, B., Puillandre, N., Aplin, K. P., Doughty, P., Hutchinson, M. N., Couloux, A., and Vidal, N. (2013). Hidden species diversity of Australian burrowing snakes (Ramphotyphlops). Biological Journal of the Linnean Society 110, 427–441.
| Hidden species diversity of Australian burrowing snakes (Ramphotyphlops).Crossref | GoogleScholarGoogle Scholar |
Meredith, R. W., Krajewski, C., Westerman, M., and Springer, M. S. (2009). Relationships and divergence among orders and families of Marsupialia. In ‘Papers in Geology, Palaeontology and Palaeostratigraphy in Honour of Michael O. Woodburne’. (Ed. L. H. Albright III). Museum of Northern Arizona Bulletin 65, 383–405. (Museum of Northern Arizona: Flagstaff, AZ.)
Meredith, R. W., Mendoza, M. A., Roberts, K. K., Westerman, M., and Springer, M. S. (2010). A phylogeny and timescale for the evolution of Pseudocheiridae (Marsupialia: Diprotodontia) in Australia and New Guinea. Journal of Mammalian Evolution 17, 75–99.
| A phylogeny and timescale for the evolution of Pseudocheiridae (Marsupialia: Diprotodontia) in Australia and New Guinea.Crossref | GoogleScholarGoogle Scholar |
Oliver, P. M., Adams, M., and Doughty, P. (2010). Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae). BMC Evolutionary Biology 10, 386.
| Molecular evidence for ten species and Oligo-Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae).Crossref | GoogleScholarGoogle Scholar |
Oliver, P. M., Smith, K. L., Laver, R. J., Doughty, P., and Adams, M. (2014a). Contrasting patterns of persistence and diversification in vicars of a widespread Australian lizard lineage (the Oedura marmorata complex). Journal of Biogeography 41, 2068–2079.
| Contrasting patterns of persistence and diversification in vicars of a widespread Australian lizard lineage (the Oedura marmorata complex).Crossref | GoogleScholarGoogle Scholar |
Oliver, P. M., Couper, P. J., and Pepper, M. (2014b). Independent transitions between monsoonal and arid biomes revealed by systematic revison of a complex of Australian geckos (Diplodactylus; Diplodactylidae). PLoS One 9, e111895.
| Independent transitions between monsoonal and arid biomes revealed by systematic revison of a complex of Australian geckos (Diplodactylus; Diplodactylidae).Crossref | GoogleScholarGoogle Scholar |
Painter, J., Krajewski, C., and Westerman, M. (1995). Molecular phylogeny of the marsupial genus Planigale (Dasyuridae). Journal of Mammalogy 76, 406–413.
| Molecular phylogeny of the marsupial genus Planigale (Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Posada, D (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=af9cf65d1a4d02e37a96bd0c98051c55CAS |
Potter, S., Eldridge, M., Taggart, D., and Cooper, S. (2012). Multiple biogeographical barriers identified across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock-wallabies. Molecular Ecology 21, 2254–2269.
| Multiple biogeographical barriers identified across the monsoon tropics of northern Australia: phylogeographic analysis of the brachyotis group of rock-wallabies.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, D. L., Darling, A, Hohne, S, Larget, B, Liu, L, Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=8b7d26e065119a1a927a6cce2070063aCAS |
Strahan, R. (1995). ‘The Mammals of Australia.’ (Reed Books: Sydney.)
Tate, G. H. H., and Archbold, R. (1941). New rodents and marsupials from New Guinea. Results of the Archbold Expeditions, No. 31. American Museum Novitates. The American Museum of Natural History 1101, 1–9.
Taylor, J. M., Calaby, J. H., and Redhead, T. D. (1982). Breeding in wild populations of the marsupial mouse Planigale maculata sinualis (Dasyuridae, Marsupialia). In ‘Carnivorous Marsupials’. (Ed. M. Archer.) pp. 83–87. (Royal Zoological Society New South Wales: Sydney.).
Thomas, O. (1906). On mammals from northern Australia presented to the National Museum by Sir William Ingram, Bt. and the Honorable John Forrest. Proceedings of the Zoological Society of London 1906, 536–543.
Thomas, O. (1926). On various mammals obtained during Capt. Wilkins’s Expedition in Australia. Annals & Magazine of Natural History 17, 625–635.
| On various mammals obtained during Capt. Wilkins’s Expedition in Australia.Crossref | GoogleScholarGoogle Scholar |
Toon, A., Hughes, J. M., and Joseph, L. (2010). Multilocus analysis of honeyeaters (Aves: Meliphagidae) highlights spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone. Molecular Ecology 19, 2980–2994.
| Multilocus analysis of honeyeaters (Aves: Meliphagidae) highlights spatio-temporal heterogeneity in the influence of biogeographic barriers in the Australian monsoonal zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyktb3F&md5=15523eab8cd31106780709a970ba21d8CAS |
Travouillon, K. J., Hand, S. J., Archer, M., and Black, K. H. (2014). Earliest modern bandicoot and bilby (Marsupialia, Peramelidae and Thylacomyidae) from the Miocene of the Riversleigh World Heritage Area, northwestern Queensland, Australia. Journal of Vertebrate Paleontology 34, 375–382.
| Earliest modern bandicoot and bilby (Marsupialia, Peramelidae and Thylacomyidae) from the Miocene of the Riversleigh World Heritage Area, northwestern Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Troughton, E. Le G. (1928). A new genus, species, and subspecies of marsupial mice (Family Dasyuridae). Records of the Australian Museum 16, 281–288.
| A new genus, species, and subspecies of marsupial mice (Family Dasyuridae).Crossref | GoogleScholarGoogle Scholar |
Van Dyck, S. M. (1995). Long-tailed planigale. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 110–111. (Reed Books: Australia.)
Van Dyck, S., and Strahan, R. (2008). ‘The Mammals of Australia.’ (Reed New Holland Press: Sydney.)
Van Dyck, S., Gynther, I., and Baker, A. (2013). ‘Field Companion to the Mammals of Australia.’ (New Holland Publishers: Sydney.)
Westerman, M., Kear, B. P., Aplin, K. P., Meredith, R. W., and Springer, M. S. (2012). Phylogenetic relationships of living and recently extinct bandicoots based on nuclear and mitochondrial DNA sequences: the evolution of a unique marsupial order. Molecular Phylogenetics and Evolution 62, 97–108.
| Phylogenetic relationships of living and recently extinct bandicoots based on nuclear and mitochondrial DNA sequences: the evolution of a unique marsupial order.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38%2FotFelug%3D%3D&md5=50f6d70fa24e5091e20bd022702d4991CAS |
Westerman, M., Krajewski, C., Kear, B. P., Meehan, L., Meredith, R. W., Emerling, C. A., and Springer, M. S. (2016). Phylogenetic relationships of dasyuromorphian marsupials revisited. Zoological Journal of the Linnean Society 176, 686–701.
| Phylogenetic relationships of dasyuromorphian marsupials revisited.Crossref | GoogleScholarGoogle Scholar |
Woodhead, J., Hand, S. J., Archer, M., Graham, I., Sniderman, K., Arena, D. A., Black, K. A., Godthelp, H., Creaser, P., and Price, E. (2016). Developing a radiometrically-dated chronologic sequence for Neogene biotic change in Australia, from the Riversleigh World Heritage Area of Queensland. Gondwana Research 29, 153–167.
| Developing a radiometrically-dated chronologic sequence for Neogene biotic change in Australia, from the Riversleigh World Heritage Area of Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVyqs7vK&md5=33ed2bf283a41f4882e4115cc7bedd5eCAS |
Woolley, P. A. (1974). Pouch of Planigale subtilissima and other dasyurid marsupials. Journal of the Royal Society of Western Australia 57, 11–15.
Woolley, P. A., and Elliott, C. (2014). Breeding in wild populations of a small dasyurid marsupial, Planigale ingrami, in north-western Queensland using a novel method for collection of specimens. Australian Mammalogy 36, 81–89.
| Breeding in wild populations of a small dasyurid marsupial, Planigale ingrami, in north-western Queensland using a novel method for collection of specimens.Crossref | GoogleScholarGoogle Scholar |