Conservation Genetics

, Volume 11, Issue 4, pp 1579–1585 | Cite as

Delineating geographic boundaries of the woolly mouse opossums, Micoureus demerarae and Micoureus paraguayanus (Didelphimorphia: Didelphidae)

  • Isabela M. G. Dias
  • Francisca C. Almeida
  • George Amato
  • Rob DeSalle
  • Cleusa G. Fonseca
Short Communication


This paper reports on molecular classification of the woolly mouse opossum, Micoureus spp., in the southeastern Atlantic Forest in Brazil, a hotspot of critically threatened biodiversity. Phylogenetic analysis and character-based diagnosis were done using DNA sequences from the mitochondrial cytochrome b gene and cytochrome c oxidase subunit I genes, and exon 6 of the nuclear dentine matrix protein 1 gene (DMP1). Although the nuclear DMP1 gene showed insufficient genetic variation for species diagnosis, the mtDNA analyses resulted in the robust grouping of samples of the M. paraguayanus/M. demerarae complex into three clades with distinct DNA sequence diagnostics for the species units in this study. The results support the species status of M. paraguayanus (Tate in Am Mus Novit 493: 1–13, 1931), which has a geographic distribution in the Atlantic Forest from the North and Northeast of Minas Gerais state in Brazil, going south along the coastal region of Brazil, to Paraguay and Argentina. Evidence of the boundary for this species and the provided diagnostics should facilitate and improve accuracy of studies that have been done in critical threatened fragments of the Atlantic Forest, especially in Minas Gerais and Bahia states, Brazil.


Atlantic Forest Cytochrome b Cytochrome c oxidase 1 Didelphidae Micoureus Phylogeny Taxonomy 



We would like to thank our colleagues from the Sackler Institute of Comparative Genomics, especially Matt Leslie; colleagues Heitor Cunha and Raquel Moura from the Mammalogy Lab of the General Biology Department of ICB-UFMG, Tudy Camara from the Museum of Natural Sciences of PUC-MG, and Cibele R. Bonvincio from INCa, Rio de Janeiro for kindly providing samples. This study is funded by the CNPq Project PELD-PERD, the CAPES Foundation (PhD. student fellowship) and the Sackler Institute for Comparative Genomics—AMNH. In addition, the AMNH authors on this paper thank the Louis and Dorothy Cullman Program in Molecular Systematics at the AMNH.

Supplementary material

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  1. Biodiversitas Fundação (2005) Lista da Fauna Brasileira Ameaçada de Extinção. Available on line. Accessed 26 Aug 2008
  2. Borisenko AV, Lim BK, Ivanova NV, Hanner RH, Herbert PDN (2008) DNA barcoding in surveys of small mammal communities: a field study in Suriname. Mol Ecol Resour 8(3):471–479CrossRefGoogle Scholar
  3. Brito D, Fonseca G (2006) Evaluation of minimum viable population size and conservation status of the long-furred woolly mouse opossum Micoureus paraguayanus: an endemic marsupial of the Atlantic Forest. Biodivers Conserv 15(5):1713–1728CrossRefGoogle Scholar
  4. Brito D, Grelle CED (2004) Effectiveness of a reserve network for the conservation of the endemic marsupial Micoureus travassosi in Atlantic Forest remnants in southeastern Brazil. Biodivers Conserv 13(13):2519–2536CrossRefGoogle Scholar
  5. Charles-Dominique P, Atramentowicz M, Gerard H et al (1981) Les mammiferes frugivores arboricoles nocturnes d’une forêt guyanaises: inter-relations plantes-animaux. Revue d’Ecologie Terre et la Vie 35:341–435Google Scholar
  6. Costa LP (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. J Biogeogr 30:71–86CrossRefGoogle Scholar
  7. Davis JI, Nixon KC (1992) Population, genetic variation, and the delimitation of phylogenetic species. Syst Biol 41(4):421–435Google Scholar
  8. Dias IMG, Amato G, Carvalho MRS et al (2008) Characterization of eight microsatellite loci in the woolly mouse opossum, Micoureus paraguayanus, isolated from Micoureus demerarae. Molecular Ecology Resources 8:345–347CrossRefGoogle Scholar
  9. Gardner LA (1993) Order didelphimorphia. In: Wilson DE, Reeder D-AM (eds) Mammal species of the World: a taxonomic and geographic reference, 2nd edn. The Jonhs Hopkins University Press, BaltimoreGoogle Scholar
  10. Gardner LA (2007) Mammals of South America. Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, ChicagoGoogle Scholar
  11. Guindon S, Gascuel O (2003) PhyML: a simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704CrossRefPubMedGoogle Scholar
  12. IUCN (2008) 2008 IUCN Red List of threatened species. Downloaded on 24 March 2009
  13. Ivanova NV, Zemlak TS, Hanner RH, Hebert PDN (2007) Universal primer cocktails for fish DNA barcoding. Mol Ecol Notes 7(4):544–548CrossRefGoogle Scholar
  14. Jansa SA, Forsman JF, Voss RS (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. Mol Phylogen Evol 38:363–380CrossRefGoogle Scholar
  15. Kumar S, Tamura K, Nei M (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefPubMedGoogle Scholar
  16. Lesson R-P (1842) Nouveau Tableau du Règne Animal: Mammifères. Arthus Bertrand, Paris, pp 186–188Google Scholar
  17. Miranda-Ribeiro A (1936) Didelphia ou Mammalia-Ovovivipara: Marsupiaes, Didelphos, Pedimanos ou Metatherios. Revista do Museu Paulista 2:245–427Google Scholar
  18. Patton JL, Costa LP (2003) Molecular phylogeography and species limits in rainforest didelphid marsupials of South America. In: Jones M, Dickman C, Archer M (eds) Predadors with pouches: the biology of carnivorous marsupials. CSIRO Publishing, CollingwoodGoogle Scholar
  19. Patton JL, dos-Reis-Maria SF, Silva NF (1996) Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytocrome-b gene. J Mammal Evol 3(1):3–29CrossRefGoogle Scholar
  20. Reig OA, Kirsch JAW, Marshall LG (1985) New conclusions on the relationships of the opossum-like marsupials, with an annotated classification of the Didelphimorphia. Ameghiniana 21:335–343Google Scholar
  21. Rozas J, Sánchez-DelBarrio JC, Messegues X, Rozas R (2003) DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  22. Smith MF, Patton JL (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149–177CrossRefGoogle Scholar
  23. Steiner C, Catzeflis FM (2004) Genetic variation and geographical structure of five mouse-sized opossums (Marsupialia, Didelphidae) throughout the Guiana region. J Biogeogr 31(6):959–973CrossRefGoogle Scholar
  24. Swofford DL (2002) PAUP*. Phylogenetic analysis using Parsimony, version 4. Sinauer AssociatesGoogle Scholar
  25. Tate GHH (1931) Brief diagnoses of twenty-six apparently new forms of Marmosa (marsupialia) from South America. Am Mus Novit 493:1–13Google Scholar
  26. Thomas O (1888) Catalogue of the Marsupialia and Monotremata in the Collection of the British Museum (Natural history). Nat Hist Mus: Lond 1888:340–341Google Scholar
  27. Thomas O (1898) Descriptions of new mammals from South America. Ann Mag Nat Hist, Zool, Bot Geol Ser. 7 2:265–275Google Scholar
  28. Thomas O (1903) On the mammals collected by Mr. A Robert at Chapada, Mato Grosso, in Brazil (Percy Sladen expedition to Central Brazil). Proc Gen Meet Sci Bus Zool Soc Lond 2:265–275Google Scholar
  29. Thomas O (1905) New neotropical Choropterus, Sciurus, Neacomys, Coendou, Proechimys, and Marmosa. Ann Mag Nat Hist, Zool, Bot Geol Ser. 7 16:308–314Google Scholar
  30. Toyosawa S, O’Huigin C, Klein J (1999) The dentin matrix protein 1 gene of prototherian and metatherian Mammals. J Mol Evol 48:160–167CrossRefPubMedGoogle Scholar
  31. Viveiros de Castro EB, Fernandez FAS (2004) Determinants of differencial extinction vulnerabilities of small mammals in Atlantic Forest fragments in Brazil. Biol Conserv 119:73–80CrossRefGoogle Scholar
  32. Voss RS, Jansa SA (2003) Phylogenetic studies on didelphid marsupials II. Nonmolecular data and new IRBP sequences: separate and combined analyses of didelphine relationships with denser taxon sampling. Bull Am Mus Nat Hist 276:1–82CrossRefGoogle Scholar
  33. Wilson DE, Reeder D-AM (2005) Mammal species of the World: a taxonomic and geographic reference. The Jonhs Hopkins University Press, BaltimoreGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Isabela M. G. Dias
    • 1
    • 2
  • Francisca C. Almeida
    • 2
  • George Amato
    • 2
  • Rob DeSalle
    • 2
  • Cleusa G. Fonseca
    • 1
  1. 1.Departamento de Biologia Geral, ICBUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Sackler Institute for Comparative GenomicsAmerican Museum of Natural HistoryNew YorkUSA

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