Advertisement

Journal of Genetics

, Volume 91, Issue 3, pp 265–277 | Cite as

Genetic and morphological variability in South American rodent Oecomys (Sigmodontinae, Rodentia): evidence for a complex of species

  • C. C. ROSA
  • T. FLORES
  • J. C. PIECZARKA
  • R. V. ROSSI
  • M. I. C. SAMPAIO
  • J. D. RISSINO
  • P. J. S. AMARAL
  • C. Y. NAGAMACHI
RESEARCH ARTICLE

Abstract

The rodent genus Oecomys (Sigmodontinae) comprises ~16 species that inhabit tropical and subtropical forests in Central America and South America. In this study specimens of Oecomys paricola Thomas, 1904 from Belém and Marajó island, northern Brazil, were investigated using cytogenetic, molecular and morphological analyses. Three karyotypes were found, two from Belém (2n = 68, fundamental number (FN) = 72 and 2n = 70, FN = 76) and a third from Marajó island (2n = 70, FN = 72). No molecular or morphological differences were found between the individuals with differing cytotypes from Belém, but differences were evident between the individuals from Belém and Marajó island. Specimens from Belém city region may represent two cryptic species because two different karyotypes are present in the absence of significant differences in morphology and molecular characteristics. The Marajó island and Belém populations may represent distinct species that have been separated for some time, and are in the process of morphological and molecular differentiation as a consequence of reproductive isolation at the geographic and chromosomal levels. Thus, the results suggest that O. paricola may be a complex of species.

Keywords

cytogenetics chromosome speciation cryptic species rodent Oecomys paricola 

Notes

Acknowledgements

C. C. Rosa is a recipient of FAPESPA Mastership Scholarship in Neurosciences and Cellular Biology; J. C. Pieczarka, M. I. C. Sampaio, C. Y. Nagamachi are CNPq Researchers; P. J. S. Amaral is a recipient of FAPESPA Doctorship Scholarship in Genetic and Molecular Biology at Laboratório de Citogenética, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Brazil. T. Flores is a recipient of CAPES Mastership Scholarship in Zoology at Laboratório de Genética e Biologia Molecular, Universidade Federal do Pará, Campus Universitário de Bragança, Pará, Brazil.

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Fundação de Amparo à Pesquisa do Estado do Pará (FAPESPA) for financial support, and the Instituto Brasileiro de Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for authorizing sample collection.

References

  1. Andrade A. F. B. and Bonvicino C. R. 2003 A new karyological variant of Oecomys (Rodentia: Sigmodontinae) and its phylogenetic relationship based on molecular data. Genome 46, 195–203.CrossRefGoogle Scholar
  2. Avise J. C. and Walker D. 1999 Species realities and numbers in sexual vertebrates: perspectives from an asexually transmitted genome. Proc. Natl. Acad. Sci. USA 96, 992–995.PubMedCrossRefGoogle Scholar
  3. Bengtsson B. O. 1980 Rates of karyotype evolution in placental mammals. Hereditas 92, 37–47.PubMedCrossRefGoogle Scholar
  4. Bradley R. D. and Baker R. J. 2001 A test of the genetic species concept: cytochrome-b sequences and mammals. J. Mammal. 82, 960–973.CrossRefGoogle Scholar
  5. Bradley R. D. and Baker R. J. 2006 Speciation in mammals and the genetic species concept. J. Mammal. 87, 643–662.PubMedCrossRefGoogle Scholar
  6. Brandt R. S. and Pessôa L. M. 1994 Intrapopulational variability in cranial characters of Oryzomys subflavus (Wagner, 1842) (Rodentia: Cricetidae), in northeastern Brazil. Zool. Anz. 233, 45–55.Google Scholar
  7. Bush G. L., Case S. M., Wilson A. C. and Patton J. L. 1977 Rapid speciation and chromosomal evolution in mammals. Proc. Natl. Acad. Sci. USA 74, 3942–3946.PubMedCrossRefGoogle Scholar
  8. Carleton M. D. and Musser G. G. 1984 Muroid rodents. In Orders and families of recent mammals of the World (ed. S. Anderson and J. K. Jones Jr), pp. 289–379. John Wiley, New York, USA.Google Scholar
  9. Carleton M. D. and Musser G. G. 1989 Systematic studies of Oryzomyine rodents (Muridae, Sigmodontinae): a synopsis of Microryzomys. Bull. Am. Mus. Nat. Hist. 191, 1–83.Google Scholar
  10. Carleton M. D., Emmons L. H. and Musser G. G. 2009 A new species of the rodent genus Oecomys (Cricetidae: Sigmodontinae, Oryzomyini) from eastern Bolivia, with emended definitions of O. concolor (Wagner) and O. mamorae (Thomas). Am. Mus. Novit. 3661, 1–32.CrossRefGoogle Scholar
  11. Catzeflis F. and Tilak M. 2009 Molecular systematic of Neotropical spiny mice (Neacomys: Sigmodontinae, Rodentia) from the Guianan Region. Mammalia 73, 239–247.CrossRefGoogle Scholar
  12. Christoff A. U., Fagundes V., Sbalqueiro I. J., Mattevi M. S. and Yonenaga-Yassuda Y. 2000 Description of new species of Akodon (Rodentia: Sigomodontinae) from southern Brazil. J. Mammal. 81, 838–851.CrossRefGoogle Scholar
  13. D’Elía G. 2003 Phylogenetics of Sigmodontinae (Rodentia, Muroidea, Cricetidae), with special reference to the akodont group, and with additional comments on historical biogeography. Cladistics 19, 307–323.CrossRefGoogle Scholar
  14. D’Elía G., Pardiñas U. F. J., Teta P. and Patton J. L. 2007 Definition and diagnosis of a new tribe of sigmodontine rodents (Cricetidae: Sigmodontinae), and a revised classification of the subfamily. Gayana 71, 187–194.Google Scholar
  15. D’Elía G., Pardiñas U. F. J., Jayat J. P. and Salazar-Bravo J. 2008 Systematics of Necromys (Rodentia, Cricetidae, Sigmodontinae): species limits and groups, with comments on historical biogeography. J. Mammal. 89, 778–790.CrossRefGoogle Scholar
  16. Emmons L. H. and Feer F. 1997 Neotropical rainforest mammals: a field guide. 2nd edition, University of Chicago, Chicago.Google Scholar
  17. Ford C. E. and Hamerton J. L. 1956 A colchicine, hypotonic-citrate, squash sequence for mammalian chromosomes. Stain. Technol. 31, 247–251.PubMedGoogle Scholar
  18. Gardner A. L. and Emmons L. 1984 Species group in Proechimys (Rodentia, Echimyidae) as indicated by karyology and bullar morphology. J. Mammal. 65, 10–25.CrossRefGoogle Scholar
  19. Gardner A. L. and Patton J. L. 1976 Karyotypic variation in oryzomyine rodents (Cricetinae) with comments on chromosomal evolution in the neotropical cricetine complex. Occ. Pap. Mus. Zool. Lousiana St. Univ. 49, 1–48.Google Scholar
  20. Geise L., Canavez F. C. and Seuánez H. N. 1998 Comparative karyology in Akodon (Rodentia, Sigmodontinae) from Southeastern Brazil. J. Hered. 89, 158–163.PubMedCrossRefGoogle Scholar
  21. Geise L., Smith M. F. and Patton J. L. 2001 Diversification in the genus Akodon (Rodentia, Sigmodontinae) in Southeastern South America: mitochondrial DNA sequence analysis. J. Mammal. 82, 92–101.CrossRefGoogle Scholar
  22. Geise L., De Moraes D. A. and Da Silva H. S. 2005 Morphometric differentiation and distributional notes of three species of Akodon (Muridae, Sigmodontinae, Akodontini) in the Atlantic Coastal area of Brazil. Arq. Mus. Nac., Rio de Janeiro 63, 63–74.Google Scholar
  23. Granjon L. and Dobigny G. 2003 The importance of cytotaxonomy in understanding the biogeography of African rodents: Lake Chad murids as an example. Mammal Rev. 33, 77–91.CrossRefGoogle Scholar
  24. Hall T. A. 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95–98.Google Scholar
  25. Hammer O., Harper D. A. T. and Ryan P. D. 2001 PAST: Paleontological Statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9.Google Scholar
  26. Hershkovitz P. 1960 Mammals of northern Colombia, preliminary report no. 8: arboreal rice rats, a systematic revision of the subgenus Oecomys, genus Oryzomys. Proc. U. S. Natl. Mus. 110, 513–568.Google Scholar
  27. Hershkovitz P. 1962 Evolution of Neotropical cricetine rodents (Muridae) with special reference to the phyllotine group. Fieldiana, Zool. 46, 1–524.Google Scholar
  28. Hershkovitz P. 1977 Living New World monkeys (Platyrrhini), 1st volume. The University of Chicago Press, Chicago.Google Scholar
  29. Hotelling H. 1931 The generalization of Student’s ratio. Ann. Math. Stat. 2, 360–378.CrossRefGoogle Scholar
  30. Howell W. M. and Black D. A. 1980 Controlled silver-straining of nuclear organizer regions with protective colloidal developer: a 1-step method. Experientia 36, 1014–1015.PubMedCrossRefGoogle Scholar
  31. Johns G. C. and Avise J. C. 1998 A comparative summary of genetic distances in the vertebrates from the mitocondrial Cytochrome-b gene. Mol. Biol. Evol. 15, 1481–1490.PubMedCrossRefGoogle Scholar
  32. Kimura M. 1980 A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120.PubMedCrossRefGoogle Scholar
  33. King M. 1987 Chromosomal rearrangements, speciation and the theoretical approach. Heredity 59, 1–6.PubMedCrossRefGoogle Scholar
  34. King M. 1993 Species evolution. The role of chromosome change. Cambridge University Press, Cambridge.Google Scholar
  35. Langguth A., Maia V. and Mattevi M. 2005 Karyology of large size Brazilian species of the genus Oecomys Thomas, 1906 (Rodentia, Muridae, Sigmodontinae). Arq. Mus. Nac., Rio de Janeiro 63, 183–190.Google Scholar
  36. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H. et al. 2007 ClustalW and ClustalX version 2. Bioinformatics 23, 2947–2948.PubMedCrossRefGoogle Scholar
  37. Maruyama T. and Imai H. T. 1981 Evolutionary rate of the mammalian karyotype. J. Theor. Biol. 90, 111–121.PubMedCrossRefGoogle Scholar
  38. McDowell Jr S. B. 1958 The greater antillean insectivores. Bull. Am. Mus. Nat. Hist. 115, 113–214.Google Scholar
  39. Milhomem S. S. R., Pieczarka J. C., Crampton W. G. R., Silva D. S., de Souza A. C. P., Carvalho Jr J. R. and Nagamachi C. Y. 2008 Chromosomal evidence for a putative cryptic species in the Gymnotus carapo species-complex (Gymnotiformes, Gymnotidae). BMC Genet. 9, 75 (doi: 10.1186/1471-2156-9-75).PubMedCrossRefGoogle Scholar
  40. Miranda G. B., Andrades-Miranda J., Oliveira L. F. B., Langguth A. and Mattevi M. S. 2007 Geographic patterns of genetic variation and conservation consequences in three South American rodents. Biochem. Genet. 45, 839–856.PubMedCrossRefGoogle Scholar
  41. Musser G. G. and Carleton M. D. 1993 Family Muridae. In Mammals species of the world (ed. D. E. Wilson and D. M. Reeder) 2nd edition, pp. 501–753. Smithsonian Institute, Washington, USA.Google Scholar
  42. Musser G. G. and Carleton M. D. 2005 Superfamily Muroidea. In Mammal species of the world a taxonomic and geographic reference (ed. D. E. Wilson and D. M. Reeder) 3rd edition, pp. 894–1531. Johns Hopkins University Press, Baltimore.Google Scholar
  43. Nagamachi C. Y., Pieczarka J. C., Milhomem S. S. R., O’Brien P. C. M., de Souza A. C. P. and Ferguson-Smith M. A. 2010 Multiple rearrangements in cryptic species of electric knifefish, Gymnotus carapo (Gymnotidae, Gymnotiformes) revealed by chromosome painting. BMC Genet. 11, 28PubMedCrossRefGoogle Scholar
  44. Patton J. L. and Da Silva M. N. F. 1995 A review of the spiny mouse genus Scolomys (Rodentia: Muridae: Sigmodontinae) with the description of a new species from the western Amazon of Brazil. Proc. Biol. Soc. Wash. 108, 319–337.Google Scholar
  45. Patton J. L. and Gardner A. L. 1972 Notes on the systematics of Proechimys (Rodentia, Echimyidade), with emphasis on Peruvian forms. Occ. Pap. Mus. Zool. Louisiana St. Univ. 44, 1–30.Google Scholar
  46. Patton J. L., Da Silva M. N. F. and Malcom J. R. 2000 Mammals of the Rio Juruá and the evolutionary and the ecological diversification of Amazonia. Bull. Am. Mus. Nat. Hist. 244, 1–306.CrossRefGoogle Scholar
  47. Pocock R. I. 1914 On the facial vibrissae of Mammalia. Proc. Zool. Soc. London 84, 889–912.CrossRefGoogle Scholar
  48. Posada D. and Crandall K. A. 1998 Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.PubMedCrossRefGoogle Scholar
  49. Reig O. A. 1980 A new fossil genus of South American cricetid rodents allied to Wiedomys, with an assessment of the Sigmodontinae. J. Zool. 192, 257–281.CrossRefGoogle Scholar
  50. Rocha R. G., Ferreira E., Costa B. M. A., Martins I. C. M., Leite Y. L. R., Costa L. P. and Fonseca C. 2011 Small mammals of the mid-Araguaia river in central Brazil, with the description of a new species of climbing rat. Zootaxa 2789, 1–34.Google Scholar
  51. Sambrook J., Fritsch E. F. and Maniatis T. 1989 Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York, USA.Google Scholar
  52. Schneider H. 2006 Métodos de análise filogenética: um guia prático. 3rd edition, Holos Editora, Sociedade Brasileira de Genética, Ribeirão Preto, Brasil.Google Scholar
  53. Seabright M. 1971 The use of proteolitic enzymes for the mapping of structural rearrangements of man. Chromosoma 36, 204–210.Google Scholar
  54. Smith M. F. and Patton J. L. 1991 Variation in mitochondrial Cytochrome-b sequence in natural populations of South American akodontine rodents (Muridae: Sigmodontinae). Mol. Biol. Evol. 8, 85–103.PubMedGoogle Scholar
  55. Smith M. F. and Patton J. L. 1993 The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for akodontine tribe. Biol. J. Linn. Soc. 50, 149–177.CrossRefGoogle Scholar
  56. Smith M. F. and Patton J. L. 1999 Phylogenetic relationships and radiation of Sigmodontinae rodents in South America: evidence from Cytochrome b. J. Mamm. Evol. 6, 89–128.CrossRefGoogle Scholar
  57. Steppan S. J. 1995 Revision of the tribe Phyllotini (Rodentia: Sigmodontinae), with a phylogenetic hypothesis for the Sigmodontinae. Fieldiana, Zool. 80, 1–112.Google Scholar
  58. Sumner A. T. 1972 A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75, 304–306.PubMedCrossRefGoogle Scholar
  59. Silva M. J. J. and Yonenaga-Yassuda Y. 1998 Karyotype and chromosomal polymorphism of an undescribed Akodon from Central Brazil, a species with the lowest diploid chromosome number in rodents. Cytogenet. Cell Genet. 81, 46–50.PubMedCrossRefGoogle Scholar
  60. Tamura K., Dudley J., Nei M. and Kumar S. 2007 MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.PubMedCrossRefGoogle Scholar
  61. Thomas O. 1906 Notes on South American rodents. II. On the allocation of certain species hitherto referred respectively to Oryzomys, Thomasomys, and Rhipidomys. Ann. Mag. Nat. Hist. 118, 442–448.Google Scholar
  62. Thomas O. 1909 New species of Oecomys and Marmosa of Amazonia. Ann. Mag. Nat. Hist. 3, 378–380.Google Scholar
  63. Voss R. S. 1988 Systematics and ecology of ichthyomyine rodents (Muroidea): patterns of morphological evolution in a small adaptative radiation. Bull. Am. Mus. Nat. Hist. 188, 259–493.Google Scholar
  64. Voss R. S. 1991 An introduction to the neotropical muroid rodent genus Zygodontomys. Bull. Am. Mus. Nat. Hist. 210, 1–113.Google Scholar
  65. Voss R. S., Lunde D. P. and Simmons N. B. 2001 The mammal of Paracou, French Guiana: a Neotropical lowland rainforest fauna part 2. Nonvolant species. Bull. Am. Mus. Nat. Hist. 263, 1–236.CrossRefGoogle Scholar
  66. Wahlert J. H. 1974 The cranial foramina of Protrogomorphus rodents: an anatomical and phylogenetic study. Bull. Mus. Comp. Zool. 146, 363–410.Google Scholar
  67. Weksler M. 2003 Phylogeny of neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Mol. Phylogenet. Evol. 29, 331–349.PubMedCrossRefGoogle Scholar
  68. Weksler M. 2006 Phylogenetic relationships of oryzomine rodents (Muroidea: Sigmodontinae): separate and combined analyses of morphological and molecular data. Bull. Am. Mus. Nat. Hist. 296, 1–149.CrossRefGoogle Scholar
  69. Weksler M., Percequillo A. R. and Voss R. S. 2006 Ten new genera of Oryzomyine rodents (Cricetidae, Sigmodontinae). Am. Mus. Novit. 3537, 1–29.CrossRefGoogle Scholar
  70. Xia X. and Xie Z. 2001 DAMBE: Software package for data analysis in molecular biology and evolution. J. Hered. 92, 371–373.PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2012

Authors and Affiliations

  • C. C. ROSA
    • 1
  • T. FLORES
    • 2
  • J. C. PIECZARKA
    • 1
  • R. V. ROSSI
    • 3
  • M. I. C. SAMPAIO
    • 2
  • J. D. RISSINO
    • 1
  • P. J. S. AMARAL
    • 1
  • C. Y. NAGAMACHI
    • 1
  1. 1.Laboratório de Citogenética, Instituto de Ciências BiológicasUniversidade Federal do ParáBelémBrazil
  2. 2.Laboratório de Genética e Biologia MolecularUniversidade Federal do Pará, Campus Universitário de BragançaParáBrazil
  3. 3.Departamento de Biologia e Zoologia, Instituto de BiociênciasUniversidade Federal do Mato GrossoMato GrossoBrazil

Personalised recommendations