Abstract
The murid rodent genus Rattus Fischer 1803 contains several species that are responsible for massive loss of crops and food, extinction of other species and the spread of zoonotic diseases to humans, as well as a laboratory species used to answer important questions in physiology, immunology, pharmacology, toxicology, nutrition, behaviour and learning. Despite the well-known significant impacts of Rattus, a definitive evolutionary based systematic framework for the genus is not yet available. The past 75 years have seen more dramatic changes in membership of Rattus than in almost any other genus of mammals. In fact, the Rattus genus has been a receptacle for any generalised Old World murine that lacked morphological specialisation and at one point, has included more than 560 species and/or subspecies, spread across Eurasia, Africa and the Australo-Papuan region. The dissolution of Rattus is ongoing as many of its constituent species and many genera of Rattini remain unsampled in any molecular study. To address this sampling limitation, we sequenced the mitochondrial cytochrome b (cytb) gene and examined phylogenetic relationships using both Bayesian and Maximum Likelihood algorithms for an expanded set of taxa within Rattus and among closely related genera. Here we place previously unsampled taxa in a phylogenetic context for the first time, including R. burrus, R. hoogerwerfi, R. lugens, and R. mindorensis within the Asian Rattus group, R. facetus within the Australo-Papuan Rattus radiation, and the undescribed ‘Bisa Rat’ described by Flannery as sister to the recently described genus Halmaheramys. We also present an exploratory foray into the wider topic of Rattus phylogenetics and propose that a reorganisation of the Rattus genus should require that it be a monophyletic group, include at least the type species R. norvegicus and R. rattus (plus their close allies); and exclude the Bandicota/Nesokia clade and other such specialised genera.
References
Aplin, K., Lunde, D. & Helgen, K. (2008) Rattus hoogerwerfi. The IUCN Red List of Threatened Species 2008.
http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T19336A8855347.enAplin, K.P., Brown, P.R., Jacob, J., Krebs, C.J. & Singleton G.R. (2003) Field methods for rodent studies in Asia and the Indo-Pacific. Australian Centre for International Agricultural Research, Canberra, 200 pp.
Aplin, K.P., Suzuki, H., Chinen, A.A., Chesser, R.T., ten Have, J., Donnellan, S.C., Austin, J., Frost, A., Gonzalez, J.P., Herbreteau, V., Catzeflis, F., Soubrier, J., Fang, Y-P., Robins, J., Matisoo-Smith, E., Bastos, A.D.S., Maryanto, I., Sinaga, M.H., Denys, C., Van Den Bussche, R.A., Conroy, C., Rowe, K. & Cooper, A. (2011) Multiple geographic origins of commensalism and complex dispersal history of black rats. PLoS ONE, 6, e26357.
https://dx.doi.org/10.1371/journal.pone.0026357
Atkinson, I.A.E. (1985) The spread of commensal species of Rattus to oceanic islands and their effects on island avifaunas. In: Moors, P.J. (Ed.), Conservation of island birds. International Council for Bird Preservation, Bristol, pp. 35–81.
Balakirev, A.E. & Rozhnov, V.V. (2012) Contribution to the species composition and taxonomic status of some Rattus inhabiting Southern Vietnam and Sundaland. Russian Journal of Theriology, 11, 33–45.
https://dx.doi.org/10.15298/rusjtheriol.11.1.03
Balakirev, A.E., Abramov, A.V., Tikhonov, A.N. & Rozhnov, V.V. (2012) Molecular phylogeny of the Dacnomys Division (Rodentia, Muridae): the taxonomic positions of Saxatilomys and Leopoldamys. Doklady Biological Sciences, 445, 251–254.
https://dx.doi.org/10.1134/S0012496612040096
Barnett, S.A. (2001) The Story of Rats: their impact on us and our impact on them. Griffin Press, Salisbury South, Australia, 216 pp.
Bastos, A.D., Nair, D., Taylor, P.J., Brettschneider, H., Kirsten, F., Mostert, E., von Maltitz, E., Lamb, J.M., van Hooft, P., Belmain, S.R., Contrafatto, G., Downs, S. & Chimimba, C.T. (2011) Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in south Africa. BMC Genetics, Feb 16, 12–26.
https://dx.doi.org/10.1186/1471-2156-12-26
Bi, K., Linderoth, T., Vanderpool, D., Good, J.M., Nielsen, R. & Moritz, C. (2013) Unlocking the vault: next-generation museum population genomics. Molecular Ecology, 22, 6018–6032.
https://dx.doi.org/10.1111/mec.12516
Buzan, E.V., Pagès, M., Michaux, J. & Krystufek, B. (2011) Phylogenetic position of the Ohiya rat (Srilankamys ohiensis) based on mitochondrial and nuclear gene sequence analysis. Zoologica Scripta, 40, 545–553.
https://dx.doi.org/10.1111/j.1463-6409.2011.00494.x
Caldarini, G., Capanna, E., Civitelli, M.V., Corti, M. & Simonetta, A. (1989) Chromosomal evolution in the subgenus Rattus (Rodentia, Muridae): karyotype analysis of two species from the Indian subregion. Mammalia, 53, 77–84.
https://dx.doi.org/10.1515/mamm.1989.53.1.77
Capanna, E. & Corti, M. (1991) Chromosomes, speciation and phylogeny in mammals. In: Ghiara, G. (Ed.), Symposium on the Evolution of Terrestrial Vertebrates: Proceedings of the International Symposium on Evolution of Terrestrial Vertebrates, Naples, June 9-11, 1988. Selected symposia and Monographs, Unione Zoologica Italiana, vol. 4. Mucchi, Modena, pp. 355–370.
Chan, K.L. (1977) Enzyme polymorphism in Malayan rats of the subgenus Rattus. Biochemical Systematics and Ecology, 5, 161–168.
https://dx.doi.org/10.1016/0305-1978(77)90045-X
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.
https://dx.doi.org/10.1016/0305-0491(79)90278-5
Cooper, A. & Poinar, H.N. (2000) Ancient DNA: Do It right or not at all. Science, 289, 1139.
https://dx.doi.org/10.1126/science.289.5482.1139b
Davis, D.H.S. (1965) Classification problems of African Muridae. Zoologica Africana, 1, 121–145.
https://dx.doi.org/10.1080/00445096.1965.11447305
Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
https://dx.doi.org/10.1186/1471-2148-7-214
Ellerman, J.R. (1941) The families and genera of living rodents. Vol. II. Family Muridae. British Museum (Natural History), London, 690 pp.
Ellerman, J.R. (1947) Notes on some Asiatic Rodents in the British Museum. Proceedings of the Zoological Society of London, 117, 259–271.
https://dx.doi.org/10.1111/j.1096-3642.1947.tb00509.x
Ellerman, J.R. (1949) The families and genera of living rodents. Vol. III. British Museum (Natural History), London, 210 pp.
Ellerman, J.R., Morrison-Scott, T.C.S. & Hayman, R.W. (1953) Southern African Mammals, 1758 to 1951: A Reclassification. British Museum (Natural History), London, 363 pp.
https://dx.doi.org/10.5962/bhl.title.113025
Ellerman, J.R. & Morrison-Scott, T.C.S. (1951) Checklist of Palaearctic and Indian mammals, 1758 to 1946. British Museum (Natural History), London, 810 pp.
Esselstyn, J.A., Achmadi, A.S., Handika, H. & Rowe, K.C. (2015) A hog-nosed shrew rat (Rodentia: Muridae) from Sulawesi Island, Indonesia. Journal of Mammalogy, 96, 895–907.
https://dx.doi.org/10.1093/jmammal/gyv093
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.
https://dx.doi.org/10.1111/zoj.12061
Flannery, T.F. (1995) Mammals of the South-West Pacific and Moluccan Islands. Reed Books, Chatswood. 464 pp.
Giarla, T.C. & Esselstyn, J.A. (2015) The challenges of resolving a rapid, recent radiation: empirical and simulated phylogenomics of Philippine shrews. Systematic Biology, 64, 727–740.
https://dx.doi.org/10.1093/sysbio/syv029
Graybeal, A. (1998) Is it better to add taxa or characters to a difficult phylogenetic problem? Systematic Biology, 47, 9–17.
https://dx.doi.org/10.1080/106351598260996
Groves, C.P. (2001) Primate Taxonomy. Smithsonian Institution Press, Washington, DC, 350 pp.
Groves, C. & Grubb, P. (2011) Ungulate taxonomy. Johns Hopkins University Press, Baltimore, 317 pp.
Hinton, M.A.C. (1918) Scientific results from the mammal survey. No. XVIII. Report on the house rats of India, Ceylon and Burma. Part I. Journal of the Bombay Natural History Society, 26, 59–88.
Jansa, S.A., Barker, F.K. & Heaney, L.R. (2006) The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Systematic Biology, 55, 73–88.
https://dx.doi.org/10.1080/10635150500431254
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
https://dx.doi.org/10.1093/bioinformatics/bts199
Kitchener, D.J., Aplin, K.P. & Boeadi. (1991a) A new species of Rattus from Gunung Mutis, South West Timor Island, Indonesia. Records of the Western Australian Museum, 15, 445–461.
Kitchener, D.J., How, R.A. & Maharadatunkamsi. (1991b) A new species of Rattus from the mountains of West Flores, Indonesia. Records of the Western Australian Museum, 15, 611–626.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33 (7), 1870–1874.
https://dx.doi.org/10.1093/molbev/msw054
Lack, J.B., Greene, D.U., Conroy, C.J., Hamilton, M.J., Braun, J.K., Mares, M.A. & Van Den Bussche, R.A. (2012) Invasion facilitates hybridization with introgression in the Rattus rattus species complex. Molecular Ecology, 21, 3545–3561.
https://dx.doi.org/10.1111/j.1365-294X.2012.05620.x
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://dx.doi.org/10.1093/molbev/mss020
Laurie, E.M.O. & Hill, J.E. (1954) List of Land mammals of New Guinea, Celebes, and adjacent islands, 1758-1952. British Museum (Natural History), London, 175 pp.
https://dx.doi.org/10.5962/bhl.title.112425
Lecompte, E., Aplin, K., Denys, C., Catzeflis, F., Chades, M. & Chevret, P. (2008) Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evolutionary Biology, 8, 199.
https://dx.doi.org/10.1186/1471-2148-8-199
Marshall, J.T. (1977) Family Muridae. Rats and mice. In: Lekagul, B. & McNeely, J.A. (Eds.), Mammals of Thailand. Association for the Conservation of Wildlife, Bangkok, pp. 396–487.
Maryanto, I., Sinaga, M.H., Achmadi, A.S. & Maharadatunkamsi. (2010) Morphometric variation of Rattus praetor (Thomas, 1888) complex from Papua, with the description of new species of Rattus from Gag Island. Treubia, 37, 25–48.
Matthey, R. (1965) Etude de cytogenetique sur les Murinae Africains appartenant aux genres Arvicanthis, Praomys et Mastomys (Rodentia). Mammalia, 29, 228–249.
https://dx.doi.org/10.1515/mamm.1965.29.2.228
Meerburg, G.M., Singleton, G.R. & Kijlstra, A. (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology, 35, 221–270.
https://dx.doi.org/10.1080/10408410902989837
Meerburg, B.G., Singleton, G.R. & Leirs, H. (2009) The year of the rat ends—time to fight hunger! Pest Management Science, 65, 351–352.
https://dx.doi.org/10.1002/ps.1718
Michaux, J., Chevret, P. & Renaud, S. (2007) Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation. Journal of Zoological Systematics and Evolutionary Research, 45, 263–279.
https://dx.doi.org/10.1111/j.1439-0469.2006.00390.x
Miller, G.S. & Hollister, N. (1921) Twenty new mammals collected by H. C. Raven in Celebes. Proceedings of the Biological Society of Washington, 34, 93–104.
Misonne, X. (1969). African and Indo-Australian Muridae: Evolutionary trends. Musée Royal de l’Afrique Centrale, Tervuren, Belgique. Annales, Serie in 8°, Sciences Zoologiques, 172, 1–219.
Misonne, X. (1974). Order Rodentia. Part 6. In: Meester, J. & Setzer, H.W. (Eds.), The mammals of Africa: an identification manual. Smithsonian Institution Press, Washington, pp 1–39.
Moore, W.S. (1997) Mitochondrial-gene trees versus nuclear-gene trees, a reply to Hoelzer. Evolution, 51, 627–629.
https://dx.doi.org/10.1111/j.1558-5646.1997.tb02452.x
Musser, G.G. (1981) Results of the Archbold Expeditions. No. 105. Notes on systematics of Indo-Malayan murid rodents, and descriptions of new genera and species from Ceylon, Sulawesi, and the Philippines. Bulletin of the American Museum of Natural History, 168 (3), 225–334.
Musser, G.G. (1986) Sundaic Rattus: definitions of Rattus baluensis and Rattus korinchi. American Museum Novitates, 2862, 1–24.
Musser, G.G. & Califia, D. (1982) Results of the Archbold Expeditions. No. 116. Identities of rats from Pulau Maratua and other islands off East Borneo. American Museum Novitates, 2726, 1–30.
Musser, G.G. & Carleton, M.D. (1993) Family Muridae. In: Wilson, D.E. & Reeder D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference. Smithsonian Institution Press, Washington, DC. Second Edition, pp. 501–755.
Musser, G.G. & Carleton, M.D. (2005) Superfamily Muroidea. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal Species of the World: A Taxonomic and Geographic Reference. Johns Hopkins University Press, Baltimore. Third Edition, pp. 894–1531.
Musser, G.G. & Heaney, L.R. (1985) Philippine Rattus: a new species from the Sulu Archipelago. American Museum Novitates, 2818, 1–32.
Musser, G.G. & Newcomb, C. (1983) Malaysian murids and the giant rat of Sumatra. Bulletin of the American Museum of Natural History, 175, 329–598.
Musser, G.G. & Newcomb, C. (1985) Definitions of Indochinese Rattus losea and a new species from Vietnam. American Museum Novitates, 2814, 1–32.
Niethammer, J. & Martens, J. (1975) Die Gattungen Rattus and Maxomys in Afghanistan und Nepal. Zeitschrift für Säugetierkunde, 40, 325–355.
Pages, M., Bazin, E., Galan, M., Chaval, Y., Claude, J., Michaux, J., Piry, S. & Cosson, J.F. (2013) Cytonuclear discordance among Southeast Asian black rats (Rattus rattus complex). Molecular Ecology, 22, 1019–1034.
https://dx.doi.org/10.1111/mec.12149
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. BMC Evolutionary Biology, 10, 184.
https://dx.doi.org/10.1186/1471-2148-10-184
Raman, R. & Sharma, T. (1977) Karyotype evolution and speciation in genus Rattus. Journal of Scientific and Industrial Research, 36, 386–404.
Rambaut, A. & Drummond, A.J. (2007) Tracer v1.4. Available from: http://beast.bio.ed.ac.uk/Tracer (accessed 1 July 2015)
Robins, J.H., Hingston, M., Matisoo-Smith, E. & Ross, H.A. (2007) Identifying Rattus species using mitochondrial DNA. Molecular Ecology Notes, 7, 717–729.
https://dx.doi.org/10.1111/j.1471-8286.2007.01752.x
Robins, J.H., McLenachan, P.A., Phillips, M.J., Craig, L., Ross, H.A. & Matisoo-Smith, E. (2008) Dating of divergences within the Rattus genus phylogeny using whole mitochondrial genomes. Molecular Phylogenetics and Evolution, 49, 460–466.
https://dx.doi.org/10.1016/j.ympev.2008.08.001
Robins, J.H., McLenachan, P.A., Phillips, M.J., McComish, B.J., Matisoo-Smith, E. & Ross, H.A. (2010) Evolutionary relationships and divergence times among the native rats of Australia. BMC Evolutionary Biology, 10, 375.
Robins, J.H., Tintinger, V., Aplin, K.P., Hingston, M., Matisoo-Smith, E., Penny, D. & Lavery, S.D. (2014) Phylogenetic species identification in Rattus highlights rapid radiation and morphological similarity of New Guinean species. PLoS ONE, 9, e98002.
https://dx.doi.org/10.1371/journal.pone.0098002
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
https://dx.doi.org/10.1093/sysbio/sys029
Rowe, K.C., Aplin, K.P., Baverstock, P.R. & Moritz, C. (2011) Recent and rapid speciation with limited morphological disparity in the genus Rattus. Systematic Biology, 60, 188–203.
https://dx.doi.org/10.1093/sysbio/syq092
Stamatakis, A. (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
https://dx.doi.org/10.1093/bioinformatics/btl446
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology, 75, 758–771.
https://dx.doi.org/10.1080/10635150802429642
Steppan, S.J., Adkins, R.M., Spinks, P.Q. & Hale, C. (2005) Multigene phylogeny of the Old World mice, Murinae, reveals distinct geographic lineages and the declining utility of mitochondrial genes compared to nuclear genes. Molecular Phylogenetics and Evolution, 37, 370–388.
https://dx.doi.org/10.1016/j.ympev.2005.04.016
Suckow, M.A., Weisbroth, S.H. & Franklin C.L. (2006) The Laboratory Rat. Academic Press, Boston, 928 pp.
Suzuki, H., Tsuchiya, K. & Takezaki, N. (2000) A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. Molecular Phylogenetics and Evolution, 15, 15–24.
https://dx.doi.org/10.1006/mpev.1999.0732
Taylor, J.M. & Horner, E. (1973) Results of the Archbold expeditions. No 98. Systematics of native Australian Rattus (Rodentia, Muridae). Bulletin of the American Museum of Natural History, 150, 1–130.
Thalmann, O., Hebler, J., Poinar, H.N., Paabo, S. & Vigilant, L. (2004) Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Molecular Ecology, 13, 321–335.
https://dx.doi.org/10.1046/j.1365-294X.2003.02070.x
Thomson, V.A., Aplin, K.P., Cooper, A., Hisheh, S., Suzuki, H., Maryanto, I., Yap, G. & Donnellan, S.C. (2014) Molecular genetic evidence for the place of origin of the Pacific Rat, Rattus exulans. PLoS ONE, 9, e91356.
https://dx.doi.org/10.1371/journal.pone.0091356
Timm, R.M., Weijola, V.S-A., Aplin, K.A., Donnellan, S.C., Flannery, T.F., Thomson, V.A. & Pine, R.H. (2016) A new species of Rattus (Rodentia: Muridae) from Manus Island, Papua New Guinea. Journal of Mammalogy, 97, 861–878.
https://dx.doi.org/10.1093/jmammal/gyw034
Verneau, O., Catzeflis, F. & Furano, A.V. (1997) Determination of the evolutionary relationships in Rattus sensu lato (Rodentia: Muridae) using L1 (LINE-1) amplification events. Journal of Molecular Evolution, 45, 424–436.
https://dx.doi.org/10.1007/PL00006247
Verneau, O., Catzeflis, F. & Furano, A.V. (1998) Determining and dating recent rodent speciation events by using L1 (LINE-1) retrotransposons. Proceedings of the National Academy of Sciences of the United States of America, 95, 11284–11289.
https://dx.doi.org/10.1073/pnas.95.19.11284
Wyatt, K.B., Campos, P.F., Gilbert, M.T.P., Kolokotronis, S-O., Hynes, W.H., DeSalle, R., Daszak, P., MacPhee, R.D.E. & Greenwood, A.D. (2008) Historical mammal extinction on Christmas Island (Indian Ocean) correlates with introduced infectious disease. PloS ONE, 3, e3602.
https://dx.doi.org/10.1371/journal.pone.0003602
Zakharov, E.V., Lobo, N.F., Nowak, C. & Hellmann, J.J. (2009) Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae). Heredity, 102, 590–599.
https://dx.doi.org/10.1038/hdy.2009.26