Sains Malaysiana 52(3)(2023): 741-755

http://doi.org/10.17576/jsm-2023-5203-05

Molecular Phylogeny of Long-Tailed Giant Rats (Muridae: Genus Leopoldamys) Based on Mitochondrial Cytochrome B Sequences

(Filogeni Molekul Tikus Gergasi Berekor Panjang (Muridae: Genus Leopoldamys) Berdasarkan Jujukan Sitokrom B Mitokondria)

MOHAMAD AZAM FIRDAUS SAARANI¹, HOI-SEN YONG¹, BADRUL MUNIR MD-ZAIN², JENNIFER A. LEONARD³ & HASMAHZAITI OMAR^1,4,*

¹Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

²Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

³Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avda. Américo Vespucio, 41092, Seville, Spain

⁴Museum of Zoology (Block J14), Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

Diserahkan: 6 April 2022/Diterima: 4 Januari 2023

Abstract

Two species of Leopoldamys long-tailed giant rats are found in Peninsular Malaysia. They are currently referred to as Leopoldamys ciliatus which inhabits montane habitat, and Leopoldamys vociferans which usually inhabits the lowland forest. To date, there is no report on the phylogenetic relationship of L. ciliatus with the other Leopoldamys taxa. The present study was carried out to determine its relationship, based on the mitochondrial cytochrome b (cyt b) gene sequence, with L. vociferans of Peninsular Malaysia and other congeners. Phylogenetic analysis shows that L. ciliatus is a sister-species to the lineage L1 of L. herberti and L. revertens, and is distantly related to L. edwardsi. L. vociferans, and L. sabanus form a distinct clade (lineage L5) from the other Leopoldamys taxa from Indochina. The Sumatra taxon currently known as L. sabanus is genetically distinct to L. vociferanswith K2P distances between 0.065 and 0.069. Contrary to previous opinions, L. herberti, L. revertens, and L. neilli of Indochina are valid species based on more than 2.5% threshold genetic distance. Both the L. edwardsi and L. neilli species complexes are represented by several sibling species. A more extensive taxon sampling from various regions (particularly Sumatra and other regions of Indonesia) as well as the use of morphological and molecular (mitogenomes or multiple genes) data sets are needed to provide a robust phylogeny and systematics. 

Keywords: Leopoldamys ciliatus; Malaysia; molecular phylogeny; Murinae; polyphyletic; Sundaland

Abstrak

Dua spesies tikus gergasi berekor panjang (genus Leopoldamys) boleh dijumpai di Semenanjung Malaysia. Ia kini dirujuk sebagai Leopoldamys ciliatus yang mendiami habitat pergunungan dan Leopoldamys vociferans yang biasanya mendiami hutan dataran rendah. Sehingga kini, tiada laporan mengenai hubungan filogenetik L. ciliatus bersama takson Leopoldamys yang lain. Kajian ini dijalankan untuk menentukan hubungan genetik tersebut berdasarkan jujukan gen mitokondria sitokrom b (cyt b), bersama L. vociferans dari Semenanjung Malaysia dan kongener lain. Analisis filogenetik mendedahkan bahawa L. ciliatus ialah spesies rapat kepada cabang keturunan L1, L. herberti dan L. revertens dan hubungan jauh dengan L. edwardsi. L. vociferans dan L. sabanus membentuk klad yang berbeza (keturunan L5) daripada takson Leopoldamys lain dari Indochina. Takson Sumatera yang kini dikenali sebagai L. sabanus secara genetik berbeza dengan L. vociferans bersama jarak K2P antara 0.065 dan 0.069. Bertentangan dengan pendapat sebelumnya, L. herberti, L. revertens dan L. neilli dari Indochina adalah spesies yang sah berdasarkan jarak genetik lebih daripada 2.5%. Kedua-dua kompleks spesies L. edwardsi dan L. neillidiwakili oleh beberapa spesies adik-beradik. Pensampelan takson yang lebih meluas dari pelbagai kawasan (terutamanya Sumatera dan kawasan lain di Indonesia) serta penggunaan set data morfologi dan molekul (mitogenom atau gen pelbagai) diperlukan untuk membentuk filogeni dan sistematik yang teguh.

Kata kunci: Filogeni molekul; Leopoldamys ciliatus; Malaysia; Murinae; polifiletik; Sundaland

RUJUKAN

Aplin, K. 2016. Leopoldamys ciliatus. The IUCN Red List of Threatened Species 2016: e.T136691A22434736. https://dx.doi.org/10.2305/IUCN.UK.20162.RLTS.T136691A22434736.en. Accessed on 02 May 2021.

Baker, R.J. & Bradley, R.D. 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87(4): 643-662.

Balakirev, A.E. & Rozhnov, V.V. 2010. Phylogenetic relationships and species composition in the genus Niviventer (Rodentia, Muridae) based on studies of the cytochrome b gene of mtDNA. Moscow University Biological Sciences Bulletin 65: 170-173.

Balakirev, A.E., Abramov, A.V. & Rozhnov, V.V. 2013. Revision of the genus Leopoldamys (Rodentia, Muridae) as inferred from morphological and molecular data, with a special emphasis on the species composition in continental Indochina. Zootaxa 3640(4): 521-549.

Balakirev, A.E., Abramov, A.V., Tikhonov, A.N. & Rozhnov, V.V. 2012. Molecular phylogeny of Dacnomys division (Rodentia, Muridae): The taxonomic positions of Saxatilomys and Leopoldamys. Doklady Biological Sciences 445: 1-4.

Bonhote, J.L. 1900. On the mammals collected during the “Skeat Expedition” to the Malay Peninsula, 1899-1900. Proceedings of Zoological Society of London 69: 869-883.

Brandelt, H.J., Forster, P. & Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37-48.

Camacho-Sanchez, M., Leonard, J.A., Fitriana, Y., Tilak, M.K. & Fabre, P.H. 2017. The generic status of Rattus annandalei (Bonhote, 1903) (Rodentia, Murinae) and its evolutionary implications. Journal of Mammalogy 98(5): 1340-1355.

Cannon, C.H., Morley, R.J. & Bush, A.B. 2009. The current refugial rainforests of Sundaland are unrepresentative of their biogeographic past and highly vulnerable to disturbance. Proceedings of the National academy of Sciences 106(27): 11188-11193.

Chan, K.L., Dhaliwal, S.S. & Yong, H.S. 1979. Protein variation and systematics of three subgenera of Malayan rats (Rodentia: Muridae, genus Rattus Fischer). Comparative Biochemistry and Physiology 64B: 329-337.

Chasen, F.N. 1940. A handlist of Malaysian mammals. Bulletin of Raffles Museum. No. 15.

Cros, E., Chattopadhyay, B., Garg, K.M., Ng, N.S., Tomassi, S., Benedick, S., Edwards, D.P. & Rheindt, F.E. 2020. Quaternary land bridges have not been universal conduits of gene flow. Molecular Ecology 29(14): 2692-2706.

Ellerman, J.R. 1947. Notes on some Asiatic rodents in the British Museum. Proceedings of Zoological Society of London 117: 259-271.

Ellerman, J.R. 1949. The Families and Genera of Living Rodents. London: British Museum (Natural History).

Fabre, P.H., Pagès, M., Musser, G.G., Fitriana, Y.S., Fjeldså, J., Jennings, A., Jønsson, K.A., Kennedy, J., Michaux, J., Semiadi, G., Supriatna, N. & Helgen, K.M. 2013. A new genus of rodent from Wallacea (Rodentia: Muridae: Murinae: Rattini), and its implication for biogeography and Indo-Pacific Rattini systematics. Zoological Journal of the Linnean Society 169: 408-447.

Forcina, G., Camacho-Sanchez, M., Tuh, F.Y., Moreno, S. & Leonard, J.A. 2021. Markers for genetic change. Heliyon 7(1).

Francis, C.M. 2008. A Field Guide to the Mammals of Thailand and South-East Asia. London: New Holland Publishers. p. 392.

Gorog, A.J., Sinaga, M.H. & Engstrom, M.D. 2004. Vicariance or dispersal? Historical biogeography of three Sunda shelf murine rodents (Maxomys surifer, Leopoldamys sabanus and Maxomys whiteheadi). Biological Journal of the Linnean Society 81: 91-109.

Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclear Acids Symposium Series 41: 95-98.

Harrison, J.L. 1966. Introduction to Mammals of Singapore and Malaya. Singapore: Malayan Nature Society.

Huelsenbeck, J.P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8): 754-755.

Irwin, D.M., Kocher, T.D. & Wilson, A.C. 1991. Evolution of cytochrome b gene of mammals. Journal of Molecular Evolution 32: 128-144.

Jahari, P.N.S., Azman, M.S., Omar, M.S.S., Gilbert, M.T.P. & Mohd Salleh, F. 2021. Characterization of the mitogenomes of long-tailed giant rat, Leopoldamys sabanus and a comparative analysis with other Leopoldamys species. Mitochondrial DNA Part B 6(2): 502-504.

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547-1549.

Latinne, A., Meynard, C.N., Herbreteau, V., Waengsothorn, S., Morand, S. & Michaux, J.R. 2015. Influence of past and future climate changes on the distribution of three Southeast Asian murine rodents. Journal of Biogeography 42(9): 1714-1726.

Latinne, A., Chaval, Y., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. 2013a. Is Leopoldamys neilli (Rodentia, Muridae) a synonym of Leopoldamys herberti? A reply to Balakirev et al. (2013a). Zootaxa 3731(4): 589-598.

Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. 2013b. Diversity and endemism of Murinae rodents in Thai limestone karsts. Systematics and Biodiversity 11(3): 323-344.

Latinne, A., Waengsothorn, S., Rojanadilok, P., Eiamampai, K., Sribuarod, K. & Michaux, J.R. 2012. Combined mitochondrial and nuclear markers revealed a deep vicariant history for Leopoldamys neilli, a cave-dwelling rodent of Thailand. PLoS ONE 7(10): e47670.

Li, H., Kong, L., Wang, K., Zhang, S., Motokawa, M., Wu, Y., Wang, W. & Li, Y. 2019. Molecular phylogeographic analyses and species delimitations reveal that Leopoldamys edwardsi (Rodentia: Muridae) is a species complex. Integrative Zoology 14(5): 494-505. 

Lim, H.C., Shakya, S.B., Harvey, M.G., Moyle, R.G., Fleischer, R.C., Braun, M.J. & Sheldon, F.H. 2020. Opening the door to greater phylogeographic inference in Southeast Asia: Comparative genomic study of five codistributed rainforest bird species using target capture and historical DNA. Ecology and Evolution 10(7): 3222-3247.

Lyon, M.W. Jr. 1916. Two new mammals from Sumatra. Proceedings of the Biological Society of Washington 29: 209-211. 

Mason, V.C., Helgen, K.M. & Murphy, W.J. 2019. Comparative phylogeography of forest-dependent mammals reveals Paleo-forest corridors throughout Sundaland. Journal of Heredity 110(2): 158-172.

Medway, L. 1983. The Wild Mammals of Malaya (Peninsular Malaysia) and Singapore. 2nd ed. Kuala Lumpur: Oxford University Press.

Medway, L. 1969. The Wild Mammals of Malaya and Offshore Islands including Singapore. Kuala Lumpur, Singapore, & London: Oxford University Press.

Medway, L. & Yong, H.S. 1976. Problems in the systematics of the rats (Muridae) of Peninsular Malaysia. Malaysian Journal of Science 4(A): 43-53.

Miller, G.S. 1900. Seven new rats collected by Dr. W.L. Abbott in Siam. Proceedings of Biological Society Washington 13: 137-150.

Musser, G.G. 1981. Notes on the systematics of Indo-Malayan murid rodents. Bulletin of American Museum of Natural History 168: 225-334.

Musser, G.G. & Carleton, M.D. 2005. Superfamily Muroidea. In Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd ed., edited by Wilson, D.E. & Reeder, D.R. Baltimore: John Hopkins University Press. pp. 894-1531.

Nicolas, V., Fabre, P., Bryja, J., Denys, C., Verheyen, E., Missoup, A.D., Olayemi, A., Katuala, P., Dudu, A., Colyn, M., Peterhans, J.K. & Demos, T. 2020. The phylogeny of the African wood mice (Muridae, Hylomyscus) based on complete mitochondrial genomes and five nuclear genes reveals their evolutionary history and undescribed diversity. Molecular Phylogenetics and Evolution 144: 106703.

Pages, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.F., Hugot, J.P., Morand, S. & Michaux, J. 2010. Revisiting the taxonomy of the Rattini tribe: A phylogeny-based delimitation of species boundaries. BioMed Central Evolutionary Biology 10: 184. doi:10.1186/1471-2148-10-184

Page, R.D.M. 1996. Tree View: An application to display phylogenetic trees on personal computers. Computers and Applied Bioscience 12: 357-358.

Pimsai, U., Pearch, M.J., Satasook, C., Bumrungsri, S. & Bates, P.J. 2014. Murine rodents (Rodentia: Murinae) of the Myanmar-Thai-Malaysian peninsula and Singapore: Taxonomy, distribution, ecology, conservation status, and illustrated identification keys. Bonn Zoological Bulletin 63: 15-114.

Robinson, H.C. & Kloss, C.B. 1916. Preliminary diagnoses of some new species and subspecies of mammals and birds obtained in Korinchi, West Sumatra, Feb.-June 1914. Journal of the Straits Branch of the Royal Asiatic Society 73: 269-278.

Saarani, M.A.F., Leonard, J.A., Md-Zain, B.M. & Omar, H. 2021. Greater bandicoot rats (Bandicota indica) are not native to Sundaland based on Deoxyribonucleic Acid (DNA) analyses. Journal of Mammalian Evolution 28: 929-938.

Salleh, M.F., Ramos-Madrigal, J., Peñaloza, F., Liu, S., Mikkel-Holger, S.S., Riddhi, P.P., Martins, R., Lenz, D., Fickel, J., Roos, C., Shamsir, M.S., Azman, M.S., Burton, K.L., Stephen, J.R., Wilting, A. & Gilbert, M.T.P. 2017. An expanded mammal mitogenome dataset from Southeast Asia. GigaScience 6(8).

Steppan, S.J. & Schenk, J.J. 2017. Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS ONE 12(8): e0183070. https://doi.org/10.1371/journal.pone.0183070

Thomas, O. 1882. Description of a new species of rat from China. Proceedings of Zoological Society of London 50: 587-588. 

Tobe, S.S., Kitchener, A.C. & Linacre, A.M.T. 2010. Recon­structing mammalian phylogenies: A detailed com­parison of the cytochrome b and cytochrome oxidase subunit I mitochondrial genes. PLoS ONE 5: e14156.

Yong, H.S. 1970. A Malayan view of Rattus edwardsi and R. sabanus (Rodentia: Muridae). Zoological Journal of the Linnean Society 49: 359-369.

Yong, H.S. 1969. Karyotypes of Malayan rats (Rodentia-Muridae, genus Rattus Fischer). Chromosoma 27(3): 245-267.

Yong, H.S. 1968. Karyotype of four Malayan rats (Muridae, Genus Rattus Fischer). Cytologia 33: 174-180.

Yong, H.S., Lim, P.E., Belabut, D.M. & Eamsobhana, P. 2013. Variation in the nucleolar organiser regions of the long-tailed giant rats (Rodentia, Muridae, genus Leopoldamys) in Malaysia. The Raffles Bulletin of Zoology 61(2): 855-859.

Zhang, B., He, K., Wan, T., Chen, P., Sun, G., Liu, S., Nguyen, T.S., Lin, L. & Jiang, X. 2016. Multi-locus phylogeny using topotype specimens sheds light on the systematics of Niviventer (Rodentia, Muridae) in China. BMC Evolutionary Biology 16(1): 1-12.

Zhu, D., Huang, J., Kang, C., Song, X., Yue, B. & Zhang, X. 2016. The complete mitochondrial genome of the Leopoldamys edwardsi (Rodentia: Muridae). Mitochondrial DNA Part A 27(3): 1882-1884.

^*Pengarang untuk surat-menyurat; email: zaiti_1978@um.edu.my