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Australian Mammalogy Australian Mammalogy Society
Journal of the Australian Mammal Society
RESEARCH ARTICLE

Phylogenetic relationships of the cuscuses (Diprotodontia : Phalangeridae) of island Southeast Asia and Melanesia based on the mitochondrial ND2 gene

Shimona Kealy https://orcid.org/0000-0002-0646-1313 A B I , Stephen C. Donnellan C D , Kieren J. Mitchell C E F , Michael Herrera C G , Ken Aplin A D , Sue O'Connor A B and Julien Louys A H
+ Author Affiliations
- Author Affiliations

A Archaeology and Natural History, College of Asia and the Pacific, The Australian National University, Acton, ACT 2601, Australia.

B ARC Centre of Excellence for Australian Biodiversity and Heritage, The Australian National University, Canberra, ACT 2601, Australia.

C School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

D South Australian Museum, Adelaide, SA 5000, Australia.

E ARC Centre of Excellence for Australian Biodiversity and Heritage, University of Adelaide, Adelaide, SA 5005, Australia.

F Australian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia.

G Archaeological Studies Program, University of the Philippines, Diliman, Quezon City, 1101, Manila, Philippines.

H Australian Research Centre for Human Evolution, Environmental Futures Research Institute, Griffith University, Nathan, Qld 4111, Australia.

I Corresponding author. Email: shimona.kealy@anu.edu.au

Australian Mammalogy 42(3) 266-276 https://doi.org/10.1071/AM18050
Submitted: 23 August 2018  Accepted: 1 October 2019   Published: 13 November 2019

Abstract

The species-level systematics of the marsupial family Phalangeridae, particularly Phalanger, are poorly understood, due partly to the family’s wide distribution across Australia, New Guinea, eastern Indonesia, and surrounding islands. In order to refine the species-level systematics of Phalangeridae, and improve our understanding of their evolution, we generated 36 mitochondrial ND2 DNA sequences from multiple species and sample localities. We combined our new data with available sequences and produced the most comprehensive molecular phylogeny for Phalangeridae to date. Our analyses (1) strongly support the monophyly of the three phalangerid subfamilies (Trichosurinae, Ailuropinae, Phalangerinae); (2) reveal the need to re-examine all specimens currently identified as ‘Phalanger orientalis’; and (3) suggest the elevation of the Solomon Island P. orientalis subspecies to species level (P. breviceps Thomas, 1888). In addition, samples of P. orientalis from Timor formed a clade, consistent with an introduction by humans from a single source population. However, further research on east Indonesian P. orientalis populations will be required to test this hypothesis, resolve inconsistencies in divergence time estimates, and locate the source population and taxonomic status of the Timor P. orientalis.

Additional keywords: molecular, New Guinea, Phalanger orientalis, Timor, translocation.


References

Amrine-Madsen, H., Scally, M., Westerman, M., Stanhope, M. J., Krajewski, C., and Springer, M. S. (2003). Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials. Molecular Phylogenetics and Evolution 28, 186–196.
Nuclear gene sequences provide evidence for the monophyly of australidelphian marsupials.Crossref | GoogleScholarGoogle Scholar | 12878458PubMed |

Aplin, K. P., and Helgen, K. M. (2010). Quaternary murid rodents of Timor. Part I: new material of Coryphomys buehleri Schaub, 1937, and description of a second species of the genus. Bulletin of the American Museum of Natural History 341, 1–80.
Quaternary murid rodents of Timor. Part I: new material of Coryphomys buehleri Schaub, 1937, and description of a second species of the genus.Crossref | GoogleScholarGoogle Scholar |

Beck, R. M. D. (2008). A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints. Journal of Mammalogy 89, 175–189.
A dated phylogeny of marsupials using a molecular supermatrix and multiple fossil constraints.Crossref | GoogleScholarGoogle Scholar |

Calaby, J. H. (1984). Foreword. In ‘Possums and Gliders’. (Eds A. P. Smith, and I. D. Hume.) pp. iii–iv. (Surrey Beatty & Australian Mammal Society: Sydney)

Clarkson, C., Jacobs, Z., Marwick, B., Fullagar, R., Wallis, L., Smith, M., Roberts, R. G., Hayes, E., Lowe, K., Carah, X., Florin, S. A., McNeil, J., Cox, D., Arnold, L. J., Hua, Q., Huntley, J., Brand, H. E. A., Manne, T., Fairbairn, A., Shulmeister, J., Lyle, L., Salinas, M., Page, M., Connell, K., Park, G., Norman, K., Murphy, T., and Pardoe, C. (2017). Human occupation of northern Australia by 65,000 years ago. Nature 547, 306–310.
Human occupation of northern Australia by 65,000 years ago.Crossref | GoogleScholarGoogle Scholar | 28726833PubMed |

Colgan, D. J., Flannery, T. F., Trimble, J., and Aplin, K. P. (1993). Electrophoretic and morphological analysis of the systematics of the Phalanger orientalis (Marsupialia) species complex in Papua New Guinea and the Solomon Islands. Australian Journal of Zoology 41, 355–378.
Electrophoretic and morphological analysis of the systematics of the Phalanger orientalis (Marsupialia) species complex in Papua New Guinea and the Solomon Islands.Crossref | GoogleScholarGoogle Scholar |

Crosby, K. (2002). Studies in the diversity and evolution of phalangeroid possums (Marsupialia; Phalangerida; Phalangeroidea). Ph.D. Thesis, University of New South Wales, Sydney.

Crosby, K. (2007). Rediagnosis of the fossil species assigned to Strigocuscus (Marsupialia, Phalangeridae), with description of a new genus and three new species. Alcheringa: An Australasian Journal of Palaeontology 31, 33–58.
Rediagnosis of the fossil species assigned to Strigocuscus (Marsupialia, Phalangeridae), with description of a new genus and three new species.Crossref | GoogleScholarGoogle Scholar |

Crosby, K., and Norris, C. (2003). Periotic morphology in the trichosurin possums Strigocuscus celebensis and Wyulda squamicaudata (Diprotodontia, Phalangeridae) and a revised diagnosis of the tribe Trichosurini. American Museum Novitates 3414, 1–14.
Periotic morphology in the trichosurin possums Strigocuscus celebensis and Wyulda squamicaudata (Diprotodontia, Phalangeridae) and a revised diagnosis of the tribe Trichosurini.Crossref | GoogleScholarGoogle Scholar |

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 15034147PubMed |

FigTree (2016). FigTree v1.4.3. Available at: http://tree.bio.ed.ac.uk/software/figtree/ [accessed January 2018].

Flannery, T. (1994). ‘Possums of the World: A Monograph of the Phalangeroidea.’ (Australian Museum/Geo Productions: Sydney.)

Flannery, T. F., and White, J. P. (1991). Animal translocation. National Geographic Research and Exploration 7, 96–113.

Flannery, T., Archer, M., and Maynes, G. (1987). The phylogenetic relationships of living phalangerids (Phalangeroidea: Marsupialia) with a suggested new taxonomy. In ‘Possums and Opossums: Studies in Evolution, V.II’. (Ed. M. Archer.) pp. 477–506. (Surrey Beatty & Royal Zoological Society of New South Wales: Sydney.)

George, G. G. (1987). Characterisation of the living species of cuscus (Marsupialia: Phalangeridae). In ‘Possums and Opossums: Studies in Evolution, V.II’. (Ed. M. Archer.) pp. 507–526. (Surrey Beatty & Royal Zoological Society of New South Wales: Sydney.)

Glover, I. (1986). Archaeology in Eastern Timor, 1966–67. Terra Australis 11, 1–241.

Groves, C. P. (2005). Order Diprotodontia. In ‘Mammal Species of the World: A Taxonomic and Geographic Reference’. 3rd edn. (Eds D. E. Wilson and D. M. Reeder.) pp. 43–70. (The Johns Hopkins University Press: Baltimore, MD.)

Hall, R. (2009). Southeast Asia’s changing palaeogeography. Blumea 54, 148–161.
Southeast Asia’s changing palaeogeography.Crossref | GoogleScholarGoogle Scholar |

Hamilton, A. T., and Springer, M. S. (1999). DNA sequence evidence for placement of the ground cuscus, Phalanger gymnotis, in the tribe Phalangerini (Marsupialia: Phalangeridae). Journal of Mammalian Evolution 6, 1–17.
DNA sequence evidence for placement of the ground cuscus, Phalanger gymnotis, in the tribe Phalangerini (Marsupialia: Phalangeridae).Crossref | GoogleScholarGoogle Scholar |

Hawkins, S., O’Connor, S., Maloney, T. R., Litster, M., Kealy, S., Fenner, J. N., Aplin, K., Boulanger, C., Brockwell, S., Willan, R., Piotto, E., and Louys, J. (2017). Oldest human occupation of Wallacea at Laili Cave, Timor-Leste, shows broad-spectrum foraging responses to late Pleistocene environments. Quaternary Science Reviews 171, 58–72.
Oldest human occupation of Wallacea at Laili Cave, Timor-Leste, shows broad-spectrum foraging responses to late Pleistocene environments.Crossref | GoogleScholarGoogle Scholar |

Heinsohn, T. E. (2001). Human influences on vertebrate zoogeography: animal translocation and biological invasions across and to the east of Wallace’s Line. In ‘Faunal and Floral Migrations and Evolution in SE Asia–Australasia’. (Eds I. Metcalfe, J. M. B. Smith, M. Morwood, and I. Davidson.) pp. 153–170. (A.A. Balkema: Lisse.)

Heinsohn, T. E. (2005). Den sites and habitats utilised by the northern common cuscus Phalanger orientalis (Marsupialia: Phalangeridae) in East Timor. Australian Mammalogy 27, 99–101.
Den sites and habitats utilised by the northern common cuscus Phalanger orientalis (Marsupialia: Phalangeridae) in East Timor.Crossref | GoogleScholarGoogle Scholar |

Heinsohn, T. E. (2010). Marsupials as introduced species: Long-term anthropogenic expansion of the marsupial frontier and its implications for zoogeographic interpretation. In ‘Altered Ecologies: Fire, climate and human influence on terrestrial landscapes. Terra Australia Vol. 32’. (Eds S. Haberle, J. Stevenson, and M. Prebble) pp.133-176. (ANU E Press: Canberra.)

Helgen, K. M., and Jackson, S. M. (2015). Family Phalangeridae (cuscuses, brush-tailed possums and scaly-tailed possum). In ‘Handbook of The Mammals of the World. Vol. 5: Monotremes and Marsupials’. (Eds D. E. Wilson, and R. A. Mittermeier.) pp. 456–497. (Lynx Edicions: Barcelona.)

Ho, S. Y., 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 | GoogleScholarGoogle Scholar | 15814826PubMed |

Kavanagh, J. R., Burk-Herrick, A., Westerman, M., and Springer, M. S. (2004). Relationships among families of Diprotodontia (Marsupialia) and the phylogenetic position of the autapomorphic honey possum (Tarsipes rostratus). Journal of Mammalian Evolution 11, 207–222.
Relationships among families of Diprotodontia (Marsupialia) and the phylogenetic position of the autapomorphic honey possum (Tarsipes rostratus).Crossref | GoogleScholarGoogle Scholar |

Kirsch, J. A. W., and Wolman, M. A. (2001). Molecular relationships of the bear cuscus, Ailurops ursinus (Marsupialia: Phalangeridae). Australian Mammalogy 23, 23–30.
Molecular relationships of the bear cuscus, Ailurops ursinus (Marsupialia: Phalangeridae).Crossref | GoogleScholarGoogle Scholar |

Kirsch, J. A., Springer, M. S., and Lapointe, F. J. (1997). DNA-hybridisation studies of marsupials and their implications for metatherian classification. Australian Journal of Zoology 45, 211–280.
DNA-hybridisation studies of marsupials and their implications for metatherian classification.Crossref | GoogleScholarGoogle Scholar |

Lanfear, R., Calcott, B., Ho, S. Y., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 22319168PubMed |

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2016). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.

Leary, T., Singadan, R., Menzies, J., Helgen, K., Wright, D., Allison, A., Hamilton, S., Salas, L., and Dickman, C. (2016a). Phalanger orientalis. The IUCN Red List of Threatened Species 2016:e.T16847A21951519.

Leary, T., Singadan, R., Menzies, J., Helgen, K., Wright, D., Allison, A., Aplin, K., Salas, L., and Dickman, C. (2016b). Phalanger vestitus. The IUCN Red List of Threatened Species 2016:e.T16850A21950723.

Leavesley, M. G., Bird, M. I., Fifield, L. K., Hausladen, P. A., Santos, G. M., and Di Tada, M. L. (2002). Buang Merabak: early evidence for human occupation in the Bismarck Archipelago, Papua New Guinea. Australian Archaeology 54, 55–57.
Buang Merabak: early evidence for human occupation in the Bismarck Archipelago, Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |

Leavesley, M. G., and Chappell, J. (2004). Buang Merabak: additional early radiocarbon evidence of the colonisation of the Bismarck Archipelago, Papua New Guinea. Antiquity 78, .

Louys, J., Kealy, S., O’Connor, S., Price, G. J., Hawkins, S., Aplin, K., Rizal, Y., Zaim, J., Mahirta, , Tanudirjo, D. A., Santoso, W. D., Hidayah, A. R., Trihascaryo, A., Wood, R., Bevitt, J., and Clark, T. (2017). Differential preservation of vertebrates in Southeast Asian caves. International Journal of Speleology 46, 379–408.
Differential preservation of vertebrates in Southeast Asian caves.Crossref | GoogleScholarGoogle Scholar |

Menzies, J. I., and Pernetta, J. C. (1986). A taxonomic revision of cuscuses allied to Phalanger orientalis (Marsupialia: Phalangeridae). Journal of Zoology 1, 551–618.
A taxonomic revision of cuscuses allied to Phalanger orientalis (Marsupialia: Phalangeridae).Crossref | GoogleScholarGoogle Scholar |

Meredith, R. W., Westerman, M., and Springer, M. S. (2009). A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes. Molecular Phylogenetics and Evolution 51, 554–571.
A phylogeny of Diprotodontia (Marsupialia) based on sequences for five nuclear genes.Crossref | GoogleScholarGoogle Scholar | 19249373PubMed |

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, 14–14 Nov. 2010’. pp. 1–8.

Mitchell, K. J., Pratt, R. C., Watson, L. N., Gibb, G. C., Llamas, B., Kasper, M., Edson, J., Hopwood, B., Male, D., Armstrong, K. N., Meyer, M., Hofreiter, M., Austin, J., Donnellan, S. C., Lee, M. S. Y., Phillips, M. J., and Cooper, A. (2014). Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Molecular Biology and Evolution 31, 2322–2330.
Molecular phylogeny, biogeography, and habitat preference evolution of marsupials.Crossref | GoogleScholarGoogle Scholar | 24881050PubMed |

Nilsson, M. A., Zheng, Y., Kumar, V., Phillips, M. J., and Janke, A. (2018). Speciation generates mosaic genomes in kangaroos. Genome Biology and Evolution 10, 33–44.
Speciation generates mosaic genomes in kangaroos.Crossref | GoogleScholarGoogle Scholar | 29182740PubMed |

Norris, C. A., and Musser, G. G. (2001). Systematic revision within Phalanger orientalis complex (Diprotodontia, Phalangeridae): a third species of lowland gray cuscus from New Guinea and Australia. American Museum Novitates 3356, 1–20.
Systematic revision within Phalanger orientalis complex (Diprotodontia, Phalangeridae): a third species of lowland gray cuscus from New Guinea and Australia.Crossref | GoogleScholarGoogle Scholar |

Nugraha, A. M. S., and Hall, R. (2018). Late Cenozoic palaeogeography of Sulawesi, Indonesia. Palaeogeography, Palaeoclimatology, Palaeoecology 490, 191–209.
Late Cenozoic palaeogeography of Sulawesi, Indonesia.Crossref | GoogleScholarGoogle Scholar |

O’Connor, S. (2015). Rethinking the Neolithic in island Southeast Asia, with particular reference to the archaeology of Timor-Leste and Sulawesi. Archipel 90, 15–47.
Rethinking the Neolithic in island Southeast Asia, with particular reference to the archaeology of Timor-Leste and Sulawesi.Crossref | GoogleScholarGoogle Scholar |

Osborne, M. J., and Christidis, L. (2002). Molecular relationships of the cuscuses, brushtail and scaly-tailed possums (Phalangerinae). Australian Journal of Zoology 50, 135–149.
Molecular relationships of the cuscuses, brushtail and scaly-tailed possums (Phalangerinae).Crossref | GoogleScholarGoogle Scholar |

Phillips, M. J., and Penny, D. (2003). The root of the mammalian tree inferred from whole mitochondrial genomes. Molecular Phylogenetics and Evolution 28, 171–185.
The root of the mammalian tree inferred from whole mitochondrial genomes.Crossref | GoogleScholarGoogle Scholar | 12878457PubMed |

Raterman, D., Meredith, R. W., Ruedas, L. A., and Springer, M. S. (2006). Phylogenetic relationships of the cuscuses and brushtail possums (Marsupialia: Phalangeridae) using the nuclear gene BRCA1. Australian Journal of Zoology 54, 353–361.
Phylogenetic relationships of the cuscuses and brushtail possums (Marsupialia: Phalangeridae) using the nuclear gene BRCA1.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, 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 | 22357727PubMed |

Ruedas, L. A., and Morales, J. C. (2005). Evolutionary relationships among genera of Phalangeridae (Metatheria: Diprotodontia) inferred from mitochondrial DNA. Journal of Mammalogy 86, 353–365.
Evolutionary relationships among genera of Phalangeridae (Metatheria: Diprotodontia) inferred from mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar |

Springer, M. S., Kirsch, J. A., Aplin, K., and Flannery, T. (1990). DNA hybridization, cladistics, and the phylogeny of phalangerid marsupials. Journal of Molecular Evolution 30, 298–311.
DNA hybridization, cladistics, and the phylogeny of phalangerid marsupials.Crossref | GoogleScholarGoogle Scholar | 2109091PubMed |

Springer, M. S., Hollar, L. J., and Burk, A. (1995). Compensatory substitutions and the evolution of the mitochondrial 12S rRNA gene in mammals. Molecular Biology and Evolution 12, 1138–1150.
| 8524047PubMed |

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |

Summerhayes, G. R. (2007). Island Melanesian pasts: a view from archaeology. In ‘Genes, Language, & Culture History in the Southwest Pacific’. (Ed. J. S. Friedlaender) pp.10-35. (Oxford University Press: New York.)

Summerhayes, G. R., Leavesley, M., Fairbairn, A., Mandui, H., Field, J., Ford, A., and Fullagar, R. (2010). Human adaptation and plant use in highland New Guinea 49,000 to 44,000 years ago. Science 330, 78–81.
Human adaptation and plant use in highland New Guinea 49,000 to 44,000 years ago.Crossref | GoogleScholarGoogle Scholar | 20929808PubMed |

Thomas, O. (1888). ‘Catalogue of the Marsupialia and Monotremata in the Collection of the British Museum.’ (British Museum (Natural History): London.)

Thomas, O. (1895). On some mammals collected by Mr. Albert Meek on Fergusson Island, D’Entrecasteaux Group. Novitates Zoologicae 2, 163–165.

Thomas, O. (1898). Descriptions of two new cuscuses (Phalanger) obtained by Dr. Loria in British New Guinea. Annali del Museo Civico di Storia Naturale di Genova 2a(19(39)), 5–8.

Wickler, S. (2001). ‘The prehistory of Buka: a stepping stone island in the northern Solomons. Terra Australis Vol. 16’. (Department of Archaeology and Natural History and Centre for Archaeological Research, Australian National University: Canberra.)

Wright, J. L., Wasef, S., Heupink, T. H., Westaway, M. C., Rasmussen, S., Pardoe, C., Fourmile, G. G., Young, M., Johnson, T., Slade, J., and Kennedy, R. (2018). Ancient nuclear genomes enable repatriation of Indigenous human remains. Science Advances 4, eaau5064.
Ancient nuclear genomes enable repatriation of Indigenous human remains.Crossref | GoogleScholarGoogle Scholar | 30585290PubMed |

Zachos, J., Pagani, M., Sloan, L., Thomas, E., and Billups, K. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693.
Trends, rhythms, and aberrations in global climate 65 Ma to present.Crossref | GoogleScholarGoogle Scholar | 11326091PubMed |

Zhang, C., Stadler, T., Klopfstein, S., Heath, T. A., and Ronquist, F. (2016). Total-evidence dating under the fossilized birth–death process. Systematic Biology 65, 228–249.
Total-evidence dating under the fossilized birth–death process.Crossref | GoogleScholarGoogle Scholar | 26493827PubMed |