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Type: Article
Published: 2018-10-29
Page range: 28–46
Abstract views: 64
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Integrative taxonomy of the Amazonian red-sided opossum Monodelphis glirina (J.A. Wagner, 1842) (Didelphimorphia: Didelphidae)

Mastozoologia/COZOO, Museu Paraense Emilio Goeldi, Campus de Pesquisa, Av. Perimetral 1901, CEP 66077-830, Belém, PA, Brazil.
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil, 4365, CEP 21045-900, Rio de Janeiro, RJ, Brazil.
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fiocruz, Av. Brasil, 4365, CEP 21045-900, Rio de Janeiro, RJ, Brazil. Divisão de Genética, Instituto Nacional de Câncer, Rua Andr Cavalcanti, 37, 4 andar, CEP 20231-050, Rio de Janeiro, RJ, Brazil.
Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università di Roma ‘La Sapienza’, CAP 00151 Rome, Italy.
Mammalia Amazon savanna Cerrado Cytochrome b pelage coloration systematics

Abstract

New records for Monodelphis glirina, a short-tailed opossum distributed throughout the Amazon region, from Humaitá, Amazonas state, and Confresa, Mato Grosso state, prompted new insights into the geographic distribution and genetic diversity of this species. One of the records extends the species range circa 350 km beyond the previous southeastern limit. Voucher specimens had their identification confirmed by morphological comparison with the holotype and corroborated by molecular data (mitochondrial gene Cytochrome b). Our analyses revealed an east-west geographic structure into two clades that could represent distinct species, M. glirina and M. maraxina. Furthermore, examination of the holotype brought to light that it was never formally linked with the voucher specimen collected by Johann Natterer.

 

References

  1. Antonelli, A., Quijada-Mascarñas A., Crawford, A.J., Bates, J.M., Velazco, P.M. & Wüster, W. (2010) Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In: Hoorn, C. & Wesselingh, F.P. (Eds.), Amazonia: landscape and species evolution: a look into the past. Wiley-Blackwell Publishing Ltd., Oxford, pp. 386–404.
    https://doi.org/10.1002/9781444306408.ch24

    Batalha-Filho, H., Pessoa, R.O., Fabre, P.-H., Fjendsä, J., Irestedt, M., Ericson, P.G.P., Silveira, L.F. & Miyaki, C.Y. (2014) Phylogeny and historical biogeography of gnateaters (Passeriformes, Conopopagidae) in the South America forests. Molecular Phylogenetics and Evolution, 79, 422–432.
    https://doi.org/10.1016/j.ympev.2014.06.025

    Bergallo, H.G. & Cerqueira, R. (1994) Reproduction and growth of the opossum Monodelphis domestica (Mammalia: Didelphidae) in northeastern Brazil. Journal of Zoology, 232, 551–563.
    https://doi.org/10.1111/j.1469-7998.1994.tb00003.x

    Cabrera, C. (1958) Catalogo de los mamíferos de America del Sur. Revista del Museo Argentino Ciencias Naturales “Bernardino Rivadavia”, Ciencias Zoologicas, 4, i–xvi + i–iv + 1–308. [dated 1957; published 27 March 1958]

    Caramaschi, F.P. (2011) Morfometria craniana, análises moleculares e filogeografia de Monodelphis domestica (Wagner, 1842) (Didelphimorphia: Didelphidae). Unpublished PhD Thesis, PPG Genética, Universidade Federal do Rio de Janeiro, Rio de Janeiro, 111 pp.

    Caramaschi, F.P., Nascimento, F.F., Cerqueira, R. & Bonvicino, C.R. (2011) Genetic diversity of wild populations of the grey short-tailed opossum, Monodelphis domestica (Didelphimorphia: Didelphidae), in Brazilian landscapes. Biological Journal of Linnean Society, 104, 251–263.
    https://doi.org/10.1111/j.1095-8312.2011.01724.x

    Carmignotto, A.P. & Monfort, T. (2006) Taxonomy and distribution of Brazilian species of Thylamys (Didelphimorphia: Didelphidae). Mammalia, 70, 126–144.
    https://doi.org/10.1515/MAMM.2006.013

    Carvalho, B.A., Oliveira, L.F.B., Langguth, A., Freygang, C.C., Ferraz, R.S. & Mattevi, M.S. (2011) Phylogenetic relationships and phylogeographic patterns in Monodelphis (Didelphimorphia: Didelphidae). Journal of Mammalogy, 92, 121–133
    https://doi.org/10.1644/10-MAMM-A-075.1

    Casado, F., Bonvicino, C., Nagle, C., Comas, B., Manzur, T., Lahoz, M. & Seuánez, H. (2010) Mitochondrial divergence between 2 populations of the Hooded Capuchin, Cebus (Sapajus) cay (Platyrrhini, Primates). Journal of Hereditas, 101, 261–269.
    https://doi.org/10.1093/jhered/esp119

    Cassens, I., Vicario, S., Waddell, V., Balchowsky, H., Van Belle, D., Ding, W., Fan, C., Mohan, R., Simoes-Lopes, P., Bastida, R., Meyer, A., Stanhope, M. & Milinkovitch, M. (2000) Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proceedings of Natural Academic Sciences, 97, 11343–11347.
    https://doi.org/10.1073/pnas.97.21.11343

    Clement, M., Snell, Q., Walke, P., Posada, D. & Crandall, K. (2002). TCS: estimating gene genealogies. Proceedings 16th International Parallel and Distributed Processing Symposium, 2, 184.
    https://doi.org/10.1109/IPDPS.2002.1016585

    Costa, L.P. (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. Journal of Biogeography, 30, 71–86.
    https://doi.org/10.1046/j.1365-2699.2003.00792.x

    Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.
    https://doi.org/10.1038/nmeth.2109

    Eiten, G. (1972) The Cerrado vegetation of Brazil. Botanical Review, 38, 201–341.
    https://doi.org/10.1007/BF02860070

    Gardner, A. (2005) Order Didelphimorphia. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal Species of the World: a taxonomic and geographic reference. 3rd Edition. Johns Hopkins University Press, Baltimore, pp. 3–18. Available from: http://www.press.jhu.edu (accessed 1 February 2018)

    Giarla, T.C., Voss, R.S. & Jansa, S.A. (2010) Species limits and phylogenetic relationships in the didelphid marsupial genus Thylamys based on mitochondrial DNA sequences and morphology. Bulletin of American Museum of Natural History, 346, 1–67.
    https://doi.org/10.1206/716.1

    Gottsberger, G. & Morawetz, W. (1986) Floristic, structural and phytogeographical analysis of the savannas of Humaitá (Amazonas). Flora, 178, 41–71.
    https://doi.org/10.1016/S0367-2530(17)30203-7

    Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.
    https://doi.org/10.1093/sysbio/syq010

    IBGE [Instituto Brasileiro de Geografia e Estatística] (1992) Shapes do Mapa de Vegetação do Brasil. IBGE, Rio de Janeiro, RJ, Brazil. Available from: http://www.dpi.inpe.br/Ambdata/mapa_sipam.php (accessed 30 February 2018)

    IBGE [Instituto Brasileiro de Geografia e Estatística] (2004) Mapa de Biomas do Brasil. 2nd Edition. Scale 1:5.000.000. IBGE, Rio de Janeiro, RJ, Brazil. Available from: https://ww2.ibge.gov.br/home/presidencia/noticias/21052004biomashtml.shtm (accessed 12 December 2017)

    IBGE [Instituto Brasileiro de Geografia e Estatística] (2017) IBGE Cidades v4.2.14. IBGE, Rio de Janeiro, RJ, Brazil. Available from: https://cidades.ibge.gov.br (accessed 12 December 2017)

    Irwin, D., Kocher, T. & Wilson, A. (1991) Evolution of the cytochrome-b gene of mammals. Journal of Molecular Evolution, 32, 128–144.
    https://doi.org/10.1007/BF02515385

    Latrubesse, E.M., Cozzuol, M., Silva-Caminha, S.A.F., Rigsby, C.A., Absy, M.L. & Jaramillo, C. (2010) The Late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth-Science Reviews, 99, 99–124.
    https://doi.org/10.1016/j.earscirev.2010.02.005

    Leigh, J.W. & Bryant, D. (2015) PopART: Full-feature software for haplotype network construction. Methods in Ecology Evolution, 6 (9), 1110–1116.
    https://doi.org/10.1111/2041-210X.12410

    Leite, R.N. & Rogers, D.S. (2013) Revisiting Amazonian phylogeography: insights into diversification hypothesis and novel perspectives. Organisms Diversity & Evolution, 13, 639–664.
    https://doi.org/10.1007/s13127-013-0140-8

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
    https://doi.org/10.1093/bioinformatics/btp187

    Manel, S., Schwartz, M.K., Luikart, G. & Taberlet, P. (2003) Landscape genetics: combining landscape ecology and population genetics. Trends in Ecology & Evolution, 18, 189–197.
    https://doi.org/10.1016/S0169-5347(03)00008-9

    Mesquita, D.O., Colli, G.R. & Vitt, L.J. (2007) Ecological release in lizard assemblages of neotropical savannas. Oecologia, 153, 185–195.
    https://doi.org/10.1007/s00442-007-0725-z

    Miranda, F.R., Casali, D.M., Perini, F.A., Machado, F.A. & Santos, F.R. (2017) Taxonomic review of the genus Cyclopes Gray, 1821 (Xenarthra: Pilosa), with the revalidation and description of new species. Zoological Journal of the Linnean Society, zlx079.
    https://doi.org/10.1093/zoolinnean/zlx079

    Miranda-Ribeiro, A. (1936) Didelphia ou Mammalia-ovovivipara. Revista do Museu Paulista, 20, 245–427.

    O’Dea, A., Lessios, H.A., Coate, A.G., Eytan, R.I., Restrepo-Moreno, S.A., Cione, A.L., Collins, L.S., Queiroz, A., Farris, D.W., Norris, R.D., Stallard, R.F., Woodburne, M.O., Aguilera, O., Aubry, M.-P., Berggren, W.A., Budd, A.F., Cozzuol, M.A., Coppard, S.E., Duque-Caro, H., Finnegan, S., Gasparini, G.M., Grossman, E.L., Johnson, K.G., Keigwin, L.D., Knowlton, N., Leigh, E.G., Leonard-Pingel, J.S., Marko, P.B., Pyenson, N.D., Rachello-Dolmen, P.G., Soibelzon, E., Soibelzon, L., Todd, J.A., Vermeij, G.J. & Jackson, J.B.C. (2016) Formation of the Isthmus of Panama. Ecology, 2, e1600883.
    https://doi.org/10.1126/sciadv.1600883

    Parada, A., Pardiñas, U.F.J., Salazar-Bravo, J., D’Elía, G. & Palma, R.E. (2013) Dating an impressive Neotropical radiation: Molecular time estimates for the Sigmodontinae (Rodentia) provide insights into its historical biogeography. Molecular phylogenetics and Evolution, 66, 960–968.
    https://doi.org/10.1016/j.ympev.2012.12.001

    Pavan, S.E. (2015) A new species of Monodelphis (Didelphimorphia: Didelphidae) from the Brazilian Atlantic Forest. American Museum Novitates, 3832, 1–15.
    https://doi.org/10.1206/3832.1

    Pavan, S.E., Jansa, S.A. & Voss, R.S. (2014) Molecular phylogeny of short-tailed opossums (Didelphidae: Monodelphis): Taxonomic implications and tests of evolutionary hypotheses. Molecular Phylogenetics and Evolution, 79, 199–214.
    https://doi.org/10.1016/j.ympev.2014.05.029

    Pavan, S.E., Jansa, S.A. & Voss, R.S. (2016) Spatiotemporal diversification of a low-vagility Neotropical vertebrate clade (short-tailed opossums, Didelphidae: Monodelphis). Journal of Biogeography, 43, 1299–1309.
    https://doi.org/10.1111/jbi.12724

    Pavan, S.E., Mendes-Oliveira, A.C. & Voss, R.S. (2017) A new species of Monodelphis (Didelphimorphia, Didelphidae) from the Brazilian Amazon. American Museum Novitates, 3872, 1–20.
    https://doi.org/10.1206/3872.1

    Pavan, S.E., Rossi, R.V. & Schneider, H. (2012) Species diversity in the Monodelphis brevicaudata complex (Didelphimorphia: Didelphidae) inferred from molecular and morphological data, with the description of a new species. Zoological Journal of Linnean Society, 165, 190–223.
    https://doi.org/10.1111/j.1096-3642.2011.00791.x

    Pavan, S.E. & Voss, R.S. (2016) A revised subgeneric classification of short-tailed opossums (Didelphidae: Monodelphis). American Museum Novitates, 3868, 1–44.
    https://doi.org/10.1206/3868.1

    Pelzeln, A. von (1883) Brasilische Säugethiere. Resultate von Johann Natterer’s Reisen in den Jahren 1817 bis 1835. Verhandlungen der Kaiserlich-Königlichen Zoologisch-botanischen Gesellschaft in Wien, 33 (Supplement), 1–140. Available from: https://archive.org/stream/brasilischesethi00pelz/brasilischesethi00pelz_djvu.txt (accessed 1 February 2018)

    Pine, R.H., Flores, D.A. & Bauer, K. (2013) The second known specimen of Monodelphis unistriata (Wagner) (Mammalia: Didelphimorphia), with redescription of the species and phylogenetic analysis. Zootaxa, 3640 (3), 425–441.
    https://doi.org/10.11646/zootaxa.3640.3.6

    Pine, R.H. & Handley Junior, C.O. (2008) Genus Monodelphis Burnett, 1830. In: Gardner, A.L. (Ed.), Mammals of South America. Vol. 1. Marsupials, xenarthrans, shrews, and bats. The University of Chicago Press, Chicago and London, pp. 82–107.

    Pires, J.M. (1973) Tipos de vegetação da Amazônia. Publicações Avulsas do Museu Paraense Emílio Goeldi, 20, 179–202.

    QGIS (2017) QGIS 2.18.9 ‘Las Palmas’. Free Software Foundation, Inc., Boston, MA. Available from: http://www.qgis.org/en/site/forusers/download.html (accessed 1 February 2018)

    Ridgway, R. (1912) Color standards and color nomenclature. Published by the author, Washington, D.C., 43 pp., LIII col. pls.
    https://doi.org/10.5962/bhl.title.144788

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
    https://doi.org/10.1093/bioinformatics/btg180

    Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1626 pp.

    Smith, M. & Patton, J. (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of Linnean Society, 50, 149–177.
    https://doi.org/10.1111/j.1095-8312.1993.tb00924.x

    Solari, S. (2010) A molecular perspective on the diversification of short- tailed opossums (Monodelphis: Didelphidae). Mastozoología Neotropical, 17, 317–333. Available from www.scielo.org.ar/pdf/mznt/v17n2/v17n2a07.pdf (accessed 20 December 2017)

    Solari, S., Pacheco, V., Vívar, E. & Emmons, L.H. (2012) A new species of Monodelphis (Mammalia: Didelphimorphia: Didelphidae) from the montane forests of central Peru. Proceedings of the Biological Society of Washington, 125, 295–307.
    https://doi.org/10.2988/11-33.1

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biological Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Thomas, O. (1888) Catalogue of the Marsupialia and Monotremata in the Collection of the British Museum (Natural History). British Museum (Natural History), London, xiv + 401 pp., 38 pls.
    https://doi.org/10.5962/bhl.title.56181

    Thomas, O. (1923) A new short-tailed opossum from Marajó, Amazonia. Annals and Magazine of Natural History, Series 12, 9, 157–157.
    https://doi.org/10.1080/00222932308632925

    Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
    https://doi.org/10.1007/978-1-4020-6754-9_3188

    USGS [United State Geological Survey] (2017) Global Ecosystems: South America. Available from: Available from: https://rmgsc.cr.usgs.gov/ecosystems/ (accessed 20 December 2017)

    van Nievelt, A.F.H. & Smith, K.K. (2005) Tooth Eruption in Monodelphis domestica and Its Significance for Phylogeny and Natural History. Journal of Mammalogy, 86, 333–341.
    https://doi.org/10.1644/BWG-224.1

    Vilela, J.F., Mello, B., Voloch, C.M. & Schrago, C.G. (2014) Sigmodontine rodents diversified in South America prior to the complete rise of the Panamanian Isthmus. Journal of Zoological Systematics and Evolutionary Research, 52, 249–256.
    https://doi.org/10.1111/jzs.12057

    Vilela, J.F., Oliveira, J.A. & Russo, C.A.M. (2015) The diversification of the genus Monodelphis and the chronology of Didephidae (Didelphimorphia). Zoological Journal of Linnean Society, 174, 414–427.
    https://doi.org/10.1111/zoj.12240

    Voss, R.S., Pine, R.H. & Solari, S. (2012) A new species of the didelphid marsupial genus Monodelphis from Bolivia. American Museum Novitates, 3740, 1–14.
    https://doi.org/10.1206/3740.2

    Wagner, J.A. (1842) Diagnosen neuer Arten brasilischer Säugthiere. Archive für Naturgeschchte, 8 (1), 356–362. Available from: https://www.biodiversitylibrary.org/page/13672551#page/382/mode/1up (accessed 30 January 2018).

    Wagner, J.A. (1847) Beiträge zur Kenntniss der Säugthiere Amerika’s. Abhandlungen der Mathematisch-Physikalische Kalsse der Königlich. Bayerische Akademie derWissenschafetn, München, 5, 121–208, 3 pls. Available from: https://opacplus.bsb-muenchen.de/Vta2/bsb10232062/bsb:BV003796813;jsessionid=39F204EA3878C783E48222581216A867.touch04?lang=en (accessed 30 January 2018)