Abstract
This study aims to clarify the taxonomic status of Monodelphis dimidiata and M. sorex, using molecular and morphometric data. Cytochrome-b sequences were obtained from specimens morphologically assignable to those taxa from the vicinity of type localities, but also representing their presumptive area of sympatry and extremes in their known distributions. These sequences were compared to GenBank downloaded sequences of select Monodelphis spp. and also of Marmosa lepida, Micoureus demerarae, and Didelphis albiventris, used as outgroups. Genetic distances and maximum likelihood analyses were performed to recover phylogenetic affinities among taxa. To access morphometric variation, univariate and multivariate statistical methods (Principal Component Analysis and Canonical Variate Analysis) were applied to the covariance matrix of 25 craniometric measurements obtained from a total of 108 specimens sampled across the geographic ranges of the species. The molecular analyses revealed a clade composed by haplotypes assignable to Monodelphis dimidiata and M. sorex (sensu Pine and Handley 2007) as distinct from the remaining Monodelphis species sampled to date, with 100% bootstrap support. Within this clade, one haplotype from Itatiaia was the sister clade to the remaining 11 specimens from Montevideo (Uruguay), Rio Grande do Sul and Santa Catarina states (Brazil), which formed an assemblage without clear geographic arrangement. In the morphometric analyses, the first two principal components of morphometric data separated variables associated with general latent size comparably expressed in all samples, and a group of variables including molars widths, molar toothrow length, and postorbital constriction breadth, which separates the geographic samples in a sequence coincident, to a large extent, with their latitudinal distributions. The sample from Itatiaia, Rio de Janeiro State, was again revealed as clearly distinct from the remaining samples, suggesting that it may represent a peripheral isolated population. With the study of original descriptions and published information on the type material of M. sorex, including photographs of syntypes, our analyses point to the recognition of M. sorex as a subjective junior synonym of M. dimidiata, which is then regarded as a widespread taxon ranging from the latitudes of southern Buenos Aires Province and Córdoba in Argentina to at least Minas Gerais State in southeastern Brazil, through the Pampas and the Atlantic Forest domains.
References
Avila–Pires, F. (1994) Mamíferos descritos do Estado do Rio Grande do Sul, Brasil. Revista Brasileira de Biologia, 54, 3, 367–384.
Azara, F. de (1801) Essais sur l’histoire naturelle des quadrupèdes de la province du Paraguay. Paris: Charles Pougens, 2 vols.
Azara, F. de (1802) Apuntamientos para la historia natural de los quadrúpedos del Paragüay y Río de la Plata, Madrid: Imprenta de la Viuda de Ibarra, 2 vols.
Bertoni A. de W. (1914) Fauna Paraguaya. Catálogos Sistemáticos de los Vertebrados del Paraguay. Peces, Batracios, Reptiles, Aves y Mamíferos Conocidos hasta 1914 In: Bertoni M. S. Descripción Física y Económica del Paraguay – M. Brossa, Asunción.
Burnett, G.T. (1830) Illustrations of the Quadrupeda, or quadrupeds, being the arrangement of the true four footed beasts indicated in the outline. Quarterly Journal of Science and Literature (1829), 28, 351.
Brown, B. (2004) Atlas of New World Marsupials Fieldiana Zoology, New Series, 102, 1–308.
Cabrera, A. (1919) Genera mammalium. Monotremata, Marsupialia. Museo Nacional de Ciencias Naturales, Madrid, 1–77, 1 unnumbered page.
de la Sancha, N., Solari, S. & Owen, R.D. (2007) First records of Monodelphis kunsi Pine (Didelphimorphia, Didelphidae) from Paraguay, with an evaluation on its distribution. Mastozoologia Neotropical, 14(2), 241–247.
Dempster, A.P., Laird, N.M. & Rubin, D.B. (1977) Maximum likelihood estimation from incomplete data via the EM algorithm. Journal of the Royal Statistical Society, B., 39, 1–38.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
Gardner, A.L. (2005) Order Didelphimorphia. Pp. 3–18. In: Mammal Species of the World, a taxonomic and geographic reference. 2vol. Third edition (Wilson, D.E. and D.M. Reeder, eds.). Smithsonian Institution Press, Washington and London, 743 pp.
Gascuel, O. (2007) BIONJ: An Improved Version of the NJ Algorithm Based on a Simple Model of Sequence Data. Molecular Biology and Evolution, 14(7), 685–695.
Gilmore, R.M. (1941) Zoology. In: The susceptibility to yellow fever of the vertebrates of eastern Colombia. I. Marsupialia (J.C. Bugher et al.), American Journal of Tropical Medicine, 21, 314–319.
Gomes, N.F. (1991) Revisão Sistemática do Gênero Monodelphis (Didelphidae: Marsupialia). Dissertação de Mestrado. IB–USP, vi+225pp.
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 2, 696–704.
Hensel, R. (1872) Beiträge zur Kenntniss der Säugethiere Süd–Brasiliens. Abhandlungen Königlich Akademie der Wissenschaften, Berlin, 1872, 1–130. Hershkovitz, P. (1959) Nomenclature and taxonomy of Neotropical mammals described by Olfers, 1818. Journal of Mammalogy, 40, 337–353.
ICZN (1999) International Code of Zoological Nomenclature, 4th ed. London: International Trust for Zoological Nomenclature.
Jansa, S.A. & Voss, R.S. (2000) Phylogenetic studies on didelphid marsupials. I. Introduction and preliminary results from nuclear IRBP gene sequences. Journal of Mammalian Evolution, 7, 43–77.
Jansa, S.A., Forsman, J.F. & Voss, R.S. (2006) Different patterns of selection on the nuclear genes IRBP and DMP–1 affect the efficiency but not the outcome of phylogeny estimation for didelphid marsupials. Molecular Phylogenetics and Evolution, 38, 363–380.
Jayat, J.P. & Miotti, M.D. (2006) Primer registro de Monodelphis kunsi (Didelphimorphia, Didelphidae) para Argentina. Mastozoología Neotropical, 12, 2, 253–256.
Lorini, M.L., Oliveira, J.A. & Person, V.G. (1994) Annual age structure and reproductive patterns in Marmosa incana (Lund, 1841) (Didelphidae, Marsupialia). Zeitschrift für Säugetierkunde, 59, 2, 65–7.
Lund, P.W. (1840) Fortsaettelse af Pattedyrene. Kongelige Danske Videnskabernes Selskabs Naturvidenskabelige og Mathematiske Afhandlinger (Royal Danish Academy of Sciences and Letters), 3, 1–56.
Mathworks (1992) Matlab Reference Guide. The Mathworks, Inc. Natick, Massachusetts, 548pp.
Miller, S.A., Dykes, D.D. & Polesky, H.F. (1988) A Simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research, 16, 3, 1215.
Miranda–Ribeiro, A. (1936) Didelphia ou Mammalia–ovovivípara – Marsupiaes, didelphos, pedimanos ou metatherios. Revista do Museu Paulista, XX, 245–427.
Nilson, M.A., Arnason, U., Spencer, P.B.S. & Janke, A. (2004) Marsupial relationships and a timeline for marsupial radiation in South Gondwana. Gene, 340, 189–196.
Olfers, I. [F. J. M.] von (1818) Bemerkugen zu Illiger’s Ueberblick der Säugthiere nach ihrer Vertheilung über die Welttheile, rücksichtlich der Südamericanischen Arten (Species). In: W. L. von Eschwege (ed.), Journal von Brasilien, oder vermischte Nachrichten aus Brasilien, auf wissenchaftlichen Reisen gesammelt: 192–237. Wimar: Im Verlage des Gr. H. S. priv. Landes-Industries-Comptoirs.
Patton, J.L., dos Reis, S.F. & Silva, M.N.F. (1996) Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome b gene. Journal of Mammalian Evolution, 3, 3–29.
Paynter Jr., R.A. (1989) Ornithological Gazetteer of Paraguay, 2nd ed. Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, iv + 64 pp.
Paynter Jr., R.A. (1995) Ornithological Gazetteer of Argentina, 2nd ed. Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, x + 1045 pp.
Paynter Jr., R.A. & Traylor Jr., M.A. (1991) Ornithological Gazetteer of Brazil (2 vols.) Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, viii + 789 pp.
Pine, R.H. (1975) A new species of Monodelphis (Mammalia: Marsupialia: Didelphidae) from Bolivia. Mammalia, 39, 2, 320–322.
Pine, R.H. (1976) Monodelphis umbristriata (A. de Miranda–Ribeiro) is a distinct species of opossum. Journal of Mammalogy, 57, 4, 785–787.
Pine, R.H. (1977) Monodelphis iheringi (Thomas) is a recognizable species of Brazilian opossum (Mammalia: Marsupialia: Didelphidae). Mammalia, 41, 2, 235–237.
Pine, R.H. (1980) Taxonomic notes on “Monodelphis dimidiata itatiayae (Miranda–Ribeiro)”, Monodelphis domestica (Wagner) and Monodelphis maraxina Thomas (Mammalia: Marsupialia: Didelphidae). Mammalia, 43, 4, 495–499.
Pine, R.H. & Abrawaya, J.P. (1978) Notes on the Brazilian opossum Monodelphis scalops (Thomas) (Mammalia: Marsupialia: Didelphidae). Mammalia, 42, 3, 379–382.
Pine, R.H. & Handley Jr., C.O. (1984) A review of the Amazonian short–tailed opossum Monodelphis emiliae (Thomas). Mammalia, 48, 2, 239–245.
Pine, R.H, Dalby, P.L. & Matson, J.O. (1985) Ecology, postnatal development, morphometrics, and taxonomic status of the short–tailed opossum, Monodelphis dimidiata, an apparently semelparous annual marsupial. Annals of Carnegie Museum, 54, 6, 195–231.
Pine, R.H. & Handley Jr., C.O. (2008) Genus Monodelphis Burnett, 1830. In: Mammals of South America. Vol.1 Marsupials, Xenarthrans, Shrews and Bats – A.L. Gardner ed., The University of Chicago Press, xx + 669pp.
Posada, D. (2003) Using MODELTEST and PAUP* to Select a Model of Nucleotide Substitution. Current Protocols in Bioinformatics, 6.5.1–6.5.14.
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics Applications Note, 14, 9, 817–818.
QIAGEN (2006) Protocol: Purification of Total DNA from Animal Tissues (Spin–Column Protocol) DNeasy Blood and Tissue Handbook, 60pp.
Rodríguez, F., Oliver, J.L., Marin, A. & Medina, J.R. (1990) The general stochastic model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.
Russo, C.A.M. (1997) Efficiencies of different statistical tests in supporting a known vertebrate phylogeny. Molecular Biology and Evolution, 14, 1078–1080.
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY), 3v.
Smith, M.F. & Patton, J.L. (1993) The diversification of South American murid rodents: Evidence from mitocondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, 50, 149–177.
Solari, S. (2007) New species of Monodelphis (Didelphimorphia: Didelphidae) from Peru, with notes on M. adusta. Journal of Mammalogy, 88, 2, 319–329.
Steiner, C. & Catzeflis, F.M. (2004) Genetic variation and geographical structure of five mouse-sized opossums (Marsupialia, Didelphidae) throughout the Guiana Region. Journal of Biogeography, 31, 6, 959–973.
Strauss, R.E, Atanassov, M.N. & Oliveira, J.A. (2003) Evaluation of the principal–component and expectation–maximization methods for estimating missing data in morphometric studies. Journal of Vertebrate Paleontology, 23, 284–296.
Swofford, D.L. (1993) “PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods), version 4.0b10”. 280p.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.
Tavaré, S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences, 17, 57–85.
Thomas, O. (1888a) Catalogue of the Marsupialia and Monotremata in the Collection of the British Museum (Natural History) Dept of Zoology, Taylor and Francis, London, 401 pp.
Thomas, O. (1888b) Diagnoses of four new species of Didelphis. Micellaneous. The Annals and Magazine of Natural History: Zoology, Botany, and Geology, 6, 1, 158–160.
USBGN (1992) Gazetteer of Argentina, Vol. I (A–L), 3rd ed. Defence Mapping Agency, Washington, DC, xxi + 722 pp.
Vargas, J., Tarifa, T. & Cortez, C. (2003) Nuevos registros de Monodelphis adusta y Monodelphis kunsi (Didelphimorphia: Didelphidae) para Bolivia. Mastozoología Neotropical, 10, 1, 123–131.
Vieira, C.O. da C. (1950) Xenartros e marsupiais do Estado de São Paulo. Arquivos de Zoologia do Estado de São Paulo, 7(4), 325–362.
Voss, R.S. & Jansa, S.A. (2009) Phylogenetic relationships and classification of didelphid marsupials, an extant radiation of New World metatherian mammals. Bulletin of the American Museum of Natural History, 322, 1–177.
Voss, R.S., Myers, P., Catzeflis, F., Carmignotto, A.P. & Barreiro, J. (2009) Chapter 11: The Six Opossums of Félix de Azara: Identification, Taxonomic History, Neotype Designations and Nomenclatural Recommentations. In: Voss, R.S. & Carleton, M.D. (eds.) Systematic Mammalogy Contributions in Honor of Guy G. Musser. Bulletin of The American Museum of Natural History, 331, 450pp.
Wagner, A. (1847) Beiträge zur Kenntniss der Säugethiere Amerika’s. Abhandlungen Mathem.–Physikalischen Classe, der Königlich Beyerischen Akademie Wissenschaften. München, 5, part, 1, 119–208.
Wetzel, R.M. & Lovett, J.W. (1974) A collection of mammals from the Chaco of Paraguay. University of Connecticut Occasional Papers Biological Science Series, 2, 203–216.
Ximénez, A., Langguth, A. & Praderi, R. (1972) Lista sistematica de los mamíferos del Uruguay. Annales del Museo Nacional de Historia Natural de Montevideo, ser. 2, 7, 5, 1–51.