Skip to main content Skip to main navigation menu Skip to site footer
Type: Articles
Published: 2011-02-09
Page range: 1–33
Abstract views: 231
PDF downloaded: 3

Geographic variation, phylogeny and systematic status of Gracilinanus microtarsus (Mammalia: Didelphimorphia: Didelphidae)

Laboratório de Mastozoologia e Biogeografia, Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Avenida Marechal Campos 1468, Maruípe, 29043-900 Vitória, ES, Brazil Corresponding author/current address: Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY 10024, USA
Laboratório de Mastozoologia e Biogeografia, Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Avenida Marechal Campos 1468, Maruípe, 29043-900 Vitória, ES, Brazil
Laboratório de Mastozoologia e Biogeografia, Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Avenida Marechal Campos 1468, Maruípe, 29043-900 Vitória, ES, Brazil
Mammalia Atlantic forest Brazil cytochrome b intraspecific variation mammal marsupials neotropics

Abstract

The gracile mouse opossum Gracilinanus microtarsus occurs mainly along the Atlantic forest of eastern and southern Brazil. Earlier studies revealed high levels of genetic divergence among samples across its range. Here, we analyzed the congruence of geographic variation between molecular and morphological characters to evaluate whether the populations that have been segregated by molecular divergence represent more than one species, as previously suggested. We examined 195 specimens of G. microtarsus, 94 of G. agilis, and 12 of Cryptonanus sp., and inferred a phylogeny based on 25 discrete morphological characters. We compared this result with a phylogeny based on partial cytochrome b sequences of 27 specimens. The monophyly of the genus, and of both G. microtarsus and G. agilis were corroborated by morphological and molecular analyses. The molecular phylogeny recovered three clades, and the morphological data indicated three distinct lineages, which also segregated in morphometric space, indicating the possibility of occurrence of three cryptic species within what is currently identified as G. microtarsus. However, morphological and molecular phylogenies were not completely congruent, and the morphological classification of the specimens included in the molecular analysis resulted in a paraphyletic group in the molecular phylogeny. Hence, our results suggest that G. microtarsus represents one species, diagnosable by morphological and molecular characters, showing strong morphological and molecular variation throughout its distributional range.

References

  1. Araujo, M.S., Martins, E.G., Cruz, L.D., Fernandes, F.R., Linhares, A.X., dos Reis, S.F. & Guimarães, P.R. Jr.. (2010) Nested diets: a novel pattern of individual-level resource use. Oikos, 119, 81–88.

    Archer, M. (1976) Basicranial region of marsupicarnivores (marsupialia), interrelationships of carnivorous marsupials, and affinities of insectivorous marsupial peramelids. Zoological Journal of the Linnean Society, 59, 1–217.

    Astúa de Moraes, D. (2004) Evolução morfológica do crânio e elementos pós-cranianos dos marsupiais americanos (Didelphimorphia, Paucituberculata, Microbiotheria). Universidade de São Paulo, São Paulo. 462 pp.

    Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T., Neigel, J.E., Reeb, C.A. & Saunders, N.C. (1987) Intraspecific phylogeography - the mitochondrial-dna bridge between population-genetics and systematics. Annual Review of Ecology and Systematics, 18, 489–522.

    Ballard, J.W.O. & Rand, D.M. (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology Evolution and Systematics, 36, 621–642.

    Bradley, R.D. & Baker, R.J. (2001) A test of the genetic species concept: Cytochrome-b sequences and mammals. Journal of Mammalogy, 82, 960–973.

    Brufford, M.W., Hanotte, O., Brookfield, J.F.Y. & Burke, T. (1992) Single locus and multilocus DNA fingerprinting. In: A. R. Hoelzel (Ed), Molecular Genetics Analysis of Populations: a Practical Approach. IRL Press, Oxford, pp. 227–229.

    Burmeister, H. (1854) Systematische uebersicht der thiere Brasiliens, welche während einer reise durch die provinzen von Rio de Janeiro und Minas Geraës gesammelt oder beobrachtet wurden von Dr. Hermann Burmeister. Säugethiere (Mammalia), I, 1–342.

    Cabrera, A. (1958) Catalogo de los mamiferos de America del Sur. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Ciencias Zoologicas, 4, 1–307.

    Cooper, C.E., Withers, P.C. & Cruz-Neto, A.P. (2009) Metabolic, Ventilatory, and Hygric Physiology of the Gracile Mouse Opossum (Gracilinanus agilis). Physiological and Biochemical Zoology, 82, 153–162.

    Costa, L.P. (2006) Filogenia de marsupiais didelfídeos e implicações para taxonomia. In: N. C. Cáceres & E. L. A. Monteiro-Filho (Eds), Os marsupiais do Brasil: biologia, ecologia e evolução. Universidade Federal do Mato Grosso do Sul, Campo Grande, pp. 667–731.

    Costa, L.P., Leite, Y.L.R. & Patton, J.L. (2003) Phylogeography and systematic notes on two species of gracile mouse opossums, genus Gracilinanus (Marsupialia : Didelphidae) from Brazil. Proceedings of the Biological Society of Washington, 116, 275–292.

    Cracraft, J. (1983) Species concepts and speciation analysis. In: R. F. Johnston (Ed), Current Ornithology.Vol. 1. Plenum Press, New York, pp. 159–187.

    Creighton, G.K. & Gardner, A.L. (2008) Genus Gracilinanus Gardner and Creighton, 1989. In: A. L. Gardner (Ed), Mammals of South America. The University of Chicago Press, Chicago and London, pp. 43–50.

    Felsenstein, J. (1985) Confidence-limits on phylogenies with a molecular clock. Systematic Zoology, 34, 152–161.

    Fernandes, F.R., Cruz, L.D., Martins, E.G. & dos Reis, S.F. (2010) Growth and home range size of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia: Didelphidae) in Brazilian cerrado. Journal of Tropical Ecology, 26, 185–192.

    Gardner, A.L. (1993) Order Didelphimorphia. In: D. E. Wilson & D. M. Reeder (Eds), Mammal species of the world. Smithsonian Institute Press, Washington, pp. 15–23.

    Gardner, A.L. (2005) Order Didelphimorphia. In: D. E. Wilson & D. M. Reeder (Eds), Mammal species of the world. Johns Hopkins University Press, Baltimore, pp. 3–18.

    Gardner, A.L. & Creighton, G.K. (1989) A new generic name for Tate's (1933) microtarsus group of South-American mouse opossums (Marsupialia, Didelphidae). Proceedings of the Biological Society of Washington, 102, 3–7.

    Geise, L. & Astúa de Moraes, D. (2009) Distribution extension and sympatric occurrence of Gracilinanus agilis and G. microtarsus (Didelphimorphia, Didelphidae), with cytogenetic notes. Biota Neotropica, 9, 1–8.

    Gray, J.E. (1821) On the natural arrangement of vertebrose animals. London Medical Repository, Montly Journal and Review, 15, 296–311.

    Gray, J.E. (1843) List of the specimens of Mammalia in the collection of the British Museum (Vol. xxviii). London: British Museum (Natural History). 216 pp.

    Grelle, C.E.V. (2003) Forest structure and vertical stratification of small mammals in a secondary Atlantic forest, southeastern Brazil. Studies on Neotropical Fauna and Environment, 38, 81–85.

    Gruber, K.F., Voss, R.S. & Jansa, S.A. (2007) Base-compositional heterogeneity in the RAG1 locus among didelphid marsupials: Implications for phylogenetic inference and the evolution of GC content. Systematic Biology, 56, 83–96.

    Hershkovitz, P. (1992) The South American gracile mouse opossum, genus Gracilinanus Gardner and Creighton, 1989 (Marmosidae, Marsupialia): a taxonomic review with notes on general morphology and relationships. Fieldiana, Zoology, 70, 1–55.

    ICZN (1999) International code of zoological nomenclature (4 ed.). London: International Trust for Zoological Nomenclature. 98 pp.

    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.

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide-sequences. Journal of Molecular Evolution, 16, 111–120.

    Kumar, S., Tamura, K. & Nei, M. (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5, 150–163.

    Langguth, A., Limeira, V.L.A.G. & Franco, S. (1997) Novo catálogo do material-tipo da coleção de mamíferos do Museu Nacional. Publicações Avulsas do Museu Nacional, 70, 1–29.

    Leite, Y.L.R., Costa, L.P. & Stallings, J.R. (1996) Diet and vertical space use of three sympatric opossums in a Brazilian Atlantic forest reserve. Journal of Tropical Ecology, 12, 435–440.

    Lesson, R.P. (1842) Nouveau tableau du regne animal mammiferes. Paris. 204 pp.

    Lew, D., Perez-Hernandez, R. & Ventura, J. (2006) Two new species of Philander (Didelphimorphia, Didelphidae) from northern South America. Journal of Mammalogy, 87, 224–237.

    Lewis, P.O. (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50, 913–925.

    Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Holmiae: Laurentii Salvii. 824 pp.

    Lund, P.W. (1840) [Preprint of] Blik paa Brasiliens Dyreverden for sidste Jordomvaeltning. Tredie Afhandling: Fortsaettelse af Pattedyrene. Kongelige Danske Videnskabernes Selskabs Naturvidenskabelige og Matematiske Afhandlinger 8, 219–272 1 pls. 14–24. [Preprint 56 pp., repaginated; not seen. Journal issue paginated as above published 1841].

    Lunde, D.P. & Schutt, W.A. (1999) The peculiar carpal tubercles of male Marmosops parvidens and Marmosa robinsoni (Didelphidae : Didelphinae). Mammalia, 63, 495–503.

    Maddison, W.P. & Maddison, D.R. (2010) Mesquite: A modular system for evolutionary analysis. version 2.74. Available from: http://mesquiteproject.org.

    Martins, E.G. & Bonato, V. (2004) On the diet of Gracilinanus microtarsus (Marsupialia, Didelphidae) in an Atlantic Rainforest fragment in southeastern Brazil. Mammalian Biology, 69, 58–60.

    Martins, E.G., Bonato, V., da-Silva, C.Q. & dos Reis, S.F. (2006a) Seasonality in reproduction, age structure and density of the gracile mouse opossum Gracilinanus microtarsus (Marsupialia : Didelphidae) in a Brazilian cerrado. Journal of Tropical Ecology, 22, 461–468.

    Martins, E.G., Bonato, V., da-Silva, C.Q. & dos Reis, S.R.F. (2006b) Partial semelparity in the neotropical didelphid marsupial Gracilinanus microtarsus. Journal of Mammalogy, 87, 915–920.

    Martins, E.G., Bonato, V., Pinheiro, A. & dos Reis, S.F. (2006c) Variation in the food-niche width of Gracilinanus microtarsus (Didelphimorphia : Didelphidae) in a cerrado remnant in south-eastern Brazil. Mammalian Biology, 71, 304–308.

    Matschie, P. (1916) Bemerkungen über die gattung Didelphis L. Sitzungsberichte der gesellschaft naturforschender freunde u Berlin, 8, 259–272.

    McKitrick, M.C. & Zink, R.M. (1988) Species concepts in ornithology. Condor, 90, 1–14.

    Miranda-Ribeiro, A.d. (1936) Didelphia ou Mammalia- Ovovivipara. Revista do Museu Paulista, 20, 245–424.

    Miranda-Ribeiro, A.d. (1955) Tipos das espécies e subespécies do Prof. Alípio de Miranda Ribeiro depositados no Museu Nacional. Arquivos do Museu Nacional, 42, 389–417.

    Mustrangi, M.A. & Patton, J.L. (1997) Phylogeography and systematics of the slender opossum Marmosops (Marsupialia, Didelphidae). University of California Publications in Zoology, 130, 1–86.

    Nichols, R. (2001) Gene trees and species trees are not the same. Trends in Ecology & Evolution, 16, 358–364.

    Passamani, M. (2000) Análise da comunidade de marsupiais em Mata Atlântica de Santa Teresa, Espírito Santo. Boletim do Museu de Biologia Mello Leitão, 11/12, 215–228.

    Patton, J.L. & Costa, L.P. (2003) Molecular phylogeography and species limits in rainforest didelphid marsupials of South America. In: M. Jones, C. Dickman & M. Archer (Eds), Predators with pouches: the biology of carnivorous marsupials. CSIRO Publishing, Collingwood, pp. 63–81.

    Patton, J.L., Da Silva, M.N.F. & Malcolm, J.R. (2000) Mammals of the Rio Jurua and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History, 244, 1–306.

    Paynter, R.A. Jr. & Traylor, M.L. Jr. (1991) Ornithological gazetteer of Brazil. Cambridge: Museum of Comparative Zoology (Harvard University). 787 pp.

    Pelzen, A.v. (1883) Brazilische Säugethiere: resultate von Johann Natterer's Reisen in den Jahren 1817 bis 1835. Verhandlugen Kaiserliche Königliche Zoologischbotanischen Gesellschaft, 33, 1–140.

    Pereira, L.G. & Geise, L. (2007) Karyotype composition of some rodents and marsupials from Chapada Diamantina (Bahia, Brazil). Brazilian Journal of Biology, 67, 509–518.

    Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Reig, O.A., Kirsch, J.A.W. & Marshall, L.G. (1987) Systematic relationships of the living and Neocenozoic american “opossum-like” marsupials (Suborder Didelphimorphia), with comments on the classification of these and of the cretaceous and Paleogene new world and european metatherians. In: M. Archer (Ed), Possums and opossums: studies in evolution. Surrey Beatty & Sons and the Royal Zoological Society of New Wales, Sydney, pp. 1–89.

    Rodriguez, F., Oliver, J.L., Marin, A. & Medina, J.R. (1990) The general stochastic-model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.

    Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Rossi, R.V., Bianconi, G.V. & Pedro, W.A. (2006) Ordem Didelphimorphia. In: N. R. Reis, A. L. Peracchi, W. A. Pedro & I. P. Lima (Eds), Mamíferos do Brasil. Secretaria de Estado do Meio Ambiente e Recursos Hídricos do Paraná, Curitiba, p. 1–437.

    Rossi, R.V., Voss, R.S. & Lunde, D.P. (2010) A revision of the didelphid marsupial genus Marmosa, part 1. The species in Tate's 'mexicana' and 'mitis' sections and other closely related forms. Bulletin of the American Museum of Natural History, 334, 1–83.

    Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., Mullis, K.B. & Erlich, H.A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA-Polymerase. Science, 239, 487–491.

    Santori, R.T. & Astúa de Moraes, D. (2006) Alimentação, nutrição e adaptações alimentares de marsupiais brasileiros. In: N. C. Cáceres & E. L. A. Monteiro-Filho (Eds), Os marsupiais do Brasil: biologia, ecologia e evolução. UNIDERP e Universidade Federal do Mato Grosso do Sul, Campo Grande, pp. 241–254.

    Smith, M.F. & Patton, J.L. (1993) The diversification of South-American murid rodents - evidence from mitochondrial-DNA sequence data for the Akodontine tribe. Biological Journal of the Linnean Society, 50, 149–177.

    Statsoft, I. (2004) STATISTICA (data analysis software system). 7.0 version. Available from: www.statsoft.com

    Swofford, D.L. (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods). In. Sinauer Associates, Sunderland.

    Tate, G.H.H. (1931) Brief diagnoses of twenty-six apparently new forms of Marmosa (Marsupialia) from South America. American Museum Novitates, 1–14.

    Tate, G.H.H. (1933) A systematic revision of the marsupial genus Marmosa, with a discussion of the adaptive radiation of the murine opossums (Marmosa). Bulletin of the American Museum of Natural History, 66, 1–246.

    Thomas, O. (1898) New mammals from Ecuador and Venezuela. Annals and Magazine of Natural History, 7, 455–456.

    Thomas, O. (1909) New species of Oecomys and Marmosa from Amazonia. Annals and Magazine of Natural History, 8, 378–380.

    Tribe, C.J. (1990) Dental age classes in Marmosa-incana and other didelphoids. Journal of Mammalogy, 71, 566–569.

    Trouessart, E.L. (1898) Catalogous mammalium tam viventium quam fossilium (Vol. II). 1238–1242.

    Vieira, E.M. (2006) Padrões de uso vertical do habitat por marsupiais brasileiros. In: N. C. Cáceres & E. L. A. Monteiro-Filho (Eds), Os marsupiais do Brasil: biologia, ecologia e evolução. Universidade Federal do Mato Grosso do Sul, Campo Grande, pp. 441–466.

    Vieira, E.M. & Astúa de Moraes, D. (2003) Carnivory and insectivory in Neotropical marsupials. In: M. Jones, C. Dickman & M. Archer (Eds), Predators with pouches: the biology os carnivorous marsupials. CSIRO Publishing, Collingwood, pp. 267–280.

    Vieira, E.M. & Izar, P. (1999) Interactions between aroids and arboreal mammals in the Brazilian Atlantic rainforest. Plant Ecology, 145, 75–82.

    Vieira, E.M. & Monteiro, E.L.A. (2003) Vertical stratification of small mammals in the Atlantic rain forest of south-eastern Brazil. Journal of Tropical Ecology, 19, 501–507.

    Vivo, M.d. (1996) How many species of mammals are there in Brazil? In: C. E. M. Bicudo & N. A. Menezes (Eds), Biodiversity in Brazil: a first approach. CNPQ, Campos do Jordão, pp. 313–321.

    Voss, R.S., Fleck, D.W. & Jansa, S.A. (2009) On the diagnostic characters, ecogeographic distribution, and phylogenetic relationships of Gracilinanus emiliae (Didelphimorphia: Didelphidae: Thylamyini). Mastozoologia Neotropical, 16, 433–443.

    Voss, R.S. & Jansa, S.A. (2003) Phylogenetic studies on didelphid marsupials II. Nonmolecular data and new IRBP sequences: Separate and combined analyses of didelphine relationships with denser taxon sampling. Bulletin of the American Museum of Natural History, 276, 1–82.

    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., Lunde, D.P. & Jansa, S.A. (2005) On the contents of Gracilinanus Gardner and Creighton, 1989, with the description of a previously unrecognized clade of small didelphid marsupials. American Museum Novitates, 3482, 1–34.

    Voss, R.S., Lunde, D.P. & Simmons, N.B. (2001) The mammals of Paracou, French Guiana: A neotropical lowland rainforest fauna - part 2. Nonvolant species. Bulletin of the American Museum of Natural History, 263, 3–236.

    Voss, R.S., Tarifa, T. & Yensen, E. (2004) An introduction to Marmosops (Marsupialia : Didelphidae), with the description of a new species from Bolivia and notes on the taxonomy and distribution of other Bolivian forms. American Museum Novitates, 3466, 1–40.

    Wagner, A. (1842) Diagnosen neuer Arten Brasilischer Saugethiere. Archiv fur Naturgeschichte, 8, 359–360.

    Weksler, M. (2006) Phylogenetic relationships of oryzomine rodents (Muroidea : Sigmodontinae): separate and combined analyses of morphological and molecular data. Bulletin of the American Museum of Natural History, 296, 3–149.

    Winge, H. (1893) Jordfundne og nulevende Pungdyr (Marsupialia) fra Lagoa Santa, Minas Geraes, Brasilien. E Museo Lundii, 2, 1–132 + 134 pls.

    Wroe, S., Ebach, M., Ahyong, S., de Muizon, C. & Muirhead, J. (2000) Cladistic analysis of dasyuromorphian (Marsupialia) phylogeny using cranial and dental characters. Journal of Mammalogy, 81, 1008–1024.