Journal of Mammalian Evolution

, Volume 6, Issue 2, pp 89–128 | Cite as

Phylogenetic Relationships and the Radiation of Sigmodontine Rodents in South America: Evidence from Cytochrome b

  • Margaret F. SmithEmail author
  • James L. Patton


Phylogenetic relationships among South American sigmodontine rodents were examined based on the complete sequence for the mitochondrial cytochrome b gene [1140 base pairs (bp)] for 66 species and between 759 and 1140 bp for an additional 19 species. Thirty-eight South American genera were represented, coming from eight of nine tribes. Outgroups included the North American murid rodents Peromyscus, Reithrodontomys, Scotinomys, and Neotoma, the Old World murine rodents Mus and Rattus, and the geomyoid genera Thomomys, Geomys, Dipodomys, and Perognathus as the most distant outgroup. The South American sigmodontines were supported as a monophyletic lineage. Within this radiation several clear-cut suprageneric groupings were identified. Many of the currently recognized tribal groupings of genera were found fairly consistently, although not always with high levels of bootstrap support. The various tribes could not be linked hierarchically with any confidence. In addition, several genera stand out as unique entities, without any apparent close relatives. The overall pattern suggests a rapid radiation of the sigmodontines in South America, followed by differentiation at the tribal and generic levels.

murid rodents Sigmodontinae mtDNA sequences cytochrome b phylogeny biogeography 


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  1. Applied Biosystems, Inc. (1994). Sequence Navigator DNA and Protein Sequence Comparison Software, Perkin-Elmer Corp., Foster City, CA.Google Scholar
  2. Baskin, J. A. (1978). Bensonomys, Calomys, and the origin of the phyllotine group of neotropical cricetines (Rodentia: Cricetidae). J. Mammal. 59: 125–135.Google Scholar
  3. Beckman, K. B., Smith, M. F., and Orrego, C. (1993). Purification of mitochondrial DNA with Wizard Minipreps DNA purification system. Promega Notes 43: 10–13.Google Scholar
  4. Bibb, M. J., Van Etten, R. A., Wright, C. T., Walberg, M. W., and Clayton, D. A. (1981). Sequence and gene organization of mouse mitochondrial DNA. Cell 26: 167–180.Google Scholar
  5. Bonvicino, C. R., and Geise, L. (1995). Taxonomic status of Delomys dorsalis collinus Thomas, 1917 (Rodentia, Cricetidae) and description of a new karyotype. Z. Säugetierkunde 60: 124–127.Google Scholar
  6. Braun, J. K. (1993). Systematic relationships of the tribe Phyllotini (Muridae: Sigmodontinae) of South America. Oklahoma Museum of Natural History. Norman.Google Scholar
  7. Braun, J. K., and Mares, M. A. (1995). A new genus and species of phyllotine rodent (Rodentia: Muridae: Sigmodontinae: Phyllotini) from South America. J. Mammal. 76: 504–521.Google Scholar
  8. Carleton, M. D. (1973). A survey of gross stomach morphology in New World Cricetinae (Rodentia, Muroidea), with comments on functional interpretations. Misc. Publ. Mus. Zool. Univ. Mich. 146: 1–43.Google Scholar
  9. Carleton, M. D. (1980). Phylogenetic relationships in neotomine-peromiscine (Muroidea) and a reappraisal of the dichotomy within New World Cricetinae. Misc. Publ. Mus. Zool. Univ. Mich. 157: 1–146.Google Scholar
  10. Catzeflis, F. M., Dickerman, A. W., Michaux, J., and Kirsch, J. A. W. (1993). DNA hybridization and rodent phylogeny. In: Mammalian Phylogeny: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 159–172, Springer-Verlag, New York.Google Scholar
  11. de Santis, L. J. M., and Justo, E. R. (1980). Akodon (Abrothrix) mansoensis, sp. nov., un nuevo “ratón lanoso” de la Provincia de Rio Negro, Argentina (Rodentia, Cricetidae). Neotropica 26: 121–127.Google Scholar
  12. Engel, S. R., Hogan, K. M., Taylor, J. F., and Davis, S. K. (1998). Molecular systematics and paleobiogeography of the South American sigmodontine rodents. Mol. Biol. Evol. 15: 35–49.Google Scholar
  13. Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27: 401–410.Google Scholar
  14. Felsenstein, J. (1981). Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Mol. Evol. 17: 368–376.Google Scholar
  15. Fonseca, G. A. B., and Kierulff, M. C. M. (1988). Biology and natural history of Brazilian Atlantic forest small mammals. Bull. Fla. State Mus. Biol. Sci. 34: 99–152.Google Scholar
  16. Gadaleta, G., Pepe, G., deCandia, G., Quagliariello, C., Sbisa, E., and Saccone, C. (1989). The complete nucleotide sequence of the Rattus norvegicus mitochondrial genome: Cryptic signals revealed by comparative analysis between vertebrates. J. Mol. Evol. 28: 497–516.Google Scholar
  17. Gardner, A. L., and Patton, J. L. (1976). Karyotypic variation in oryzomyine rodents (Cricetinae) with comments on chromosomal evolution in the neotropical cricetine complex. Occas. Papers Mus. Zool. LSU 49: 1–48.Google Scholar
  18. Graybeal, A. (1998). Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47: 9–17.Google Scholar
  19. Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 21: 160–174.Google Scholar
  20. Hendy, M. D., and Penny, D. (1989). A framework for the quantitative study of evolutionary trees. Syst. Zool. 38: 297–309.Google Scholar
  21. Hershkovitz, P. (1955). South American marsh rats, genus Holochilus, with a summary of sigmodont rodents. Fieldiana Zool. 37: 639–673.Google Scholar
  22. Hershkovitz, P. (1959). Two new genera of South American rodents (Cricetinae). Proc. Biol. Soc. Wash. 72: 5–9.Google Scholar
  23. Hershkovitz, P. (1962). Evolution of Neotropical cricetine rodents (Muridae) with special reference to the phyllotine group. Fieldiana Zool. 46: 1–524.Google Scholar
  24. Hershkovitz, P. (1966). South American swamp and fossorial rats of the scapteromyine group (Cricetinae, Muridae) with comments on the glans penis in murid taxonomy. Z. Säugetierkunde 31: 81–149.Google Scholar
  25. Hershkovitz, P. (1972). The recent mammals of the Neotropical region: A zoogeographic and ecological review. In: Evolution, Mammals, and Southern Continents, A. Keast, F. C. Erk, and B. Glass, eds., pp. 311–431, State University Press, Albany, NY.Google Scholar
  26. Hershkovitz, P. (1993). A new central Brazilian genus and species of sigmodontine rodent (Sigmodontinae) transitional between akodonts and oryzomyines, with a discussion of muroid molar morphology and evolution. Fieldiana Zool. 75: 1–18.Google Scholar
  27. Hershkovitz, P. (1998). Report on some sigmodontine rodents collected in southeastern Brazil with descriptions of a new genus and six new species. Bonn. Zool. Beitr. 47: 193–256.Google Scholar
  28. Hillis, D. M. (1998). Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst. Biol. 47: 3–8.Google Scholar
  29. Hills, D. M., and Huelsenbeck, J. P. (1992). Signal, noise, and reliability in molecular phylogenetic analyses. J. Hered. 83: 189–195.Google Scholar
  30. Hillis, D. M., and Mable, B. K., and Moritz, C. (1996). Applications of molecular systematics: The state of the field and a look to the future. In: Molecular Systematics, D. M. Hillis, C. Moritz, and B. K. Mable, eds., pp. 515–543, Sinauer Associates, Sunderland, MA.Google Scholar
  31. Hinojosa, F., Anderson, S., and Patton, J. L. (1987). Two new species of Oxymycterus (Rodentia) from Peru and Bolivia. Am. Mus. Novitates 2898: 1–17.Google Scholar
  32. Hooper, E. T., and Musser, G. G. (1964). The glans penis in neotropical cricetines (family Muridae) with comments on classification of muroid rodents. Misc. Publ. Mus. Zool. Univ. Mich. 123: 1–57.Google Scholar
  33. Huelsenbeck, J. P., and Crandall, K. A. (1997). Phylogeny estimation and hypothesis testing using maximum likelihood. Annu. Rev. Ecol. Syst. 28: 437–466.Google Scholar
  34. Irwin, D. M., Kocher, T. D., and Wilson, A. C. (1991). Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128–144.Google Scholar
  35. Jukes, T. H., and Cantor, C. R. (1969). Evolution of protein molecules. In: Mammalian Protein Molecules, H. N. Munro, ed., pp. 21–132, Academic Press, New York.Google Scholar
  36. 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.Google Scholar
  37. Kishino, H., and Hasegawa, M. (1989). Evaluation of the maximum likelihood estimate of the evolutionary tree topology from DNA sequence data, and the branching order in Hominoidea. J. Mol. Evol. 29: 170–179.Google Scholar
  38. Kumar, S., Tamura, K., and Nei, M. (1993). MEGA: Molecular Evolutionary Genetics Analysis, Version 1.01, Pennsylvania State University, University Park.Google Scholar
  39. Lansman, R. A., Shade, R. O., Shapira, J. F., and Avise, J. C. (1981). The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. III. Techniques and potential applications. J. Mol. Evol. 17: 214–226.Google Scholar
  40. Lara, M. C., Patton, J. L., and da Silva, M. N. F. (1996). The simultaneous diversification of South American echimyid rodents (Histricognathi) based on complete cytochrome b sequences. Mol. Phylogenet. Evol. 5: 403–413.Google Scholar
  41. Lessa, E. P., and Cook, J. A. (1998). The molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation. Mol. Phylogenet. Evol. 9: 88–99.Google Scholar
  42. Liascovich, R. C., Bárquez, R. M., and Reig, O. A. (1989). A karyological and morphological reassessment of Akodon (Abrothrix) illuteus Thomas. J. Mammal. 70: 386–391.Google Scholar
  43. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982). Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.Google Scholar
  44. Marshall, L. G. (1979). A model for paleobiogeography of South American cricetine rodents. Paleobiology 5: 126–132.Google Scholar
  45. Massoia, E., and Pardiñas, U. F. (1993). El estado sistematico de algunos muroideos estudiados por Ameghino en 1889. Revalidacion del genero Necromys (Mammalia, Rodentia, Cricetidae). Ameghiniana 30: 407–418.Google Scholar
  46. Medrano, J. F., Aasen, E., and Sharrow, L. (1990). DNA extraction from nucleated red blood cells. Biotechniques 8: 43.Google Scholar
  47. Musser, G. M., and Carleton, M. D. (1993). Family Muridae. In: Mammal Species of the World: A Taxonomic and Geographic Reference, D. E. Wilson and D. M. Reeder, eds., pp. 501–756, Smithsonian Institution, Washington, DC.Google Scholar
  48. Musser, G. G., Carleton, M. D., Brothers, E. M., and Gardner, A. L. (1998). Systematic studies of oryzomyine rodents (Muridae, Sigmodontinae): Diagnoses and distributions of species formerly assigned to Oryzomys “capito.” Bull. Am. Mus. Nat. Hist. 236: 1–376.Google Scholar
  49. Pardiñas, U. F. J., and Tonni, E. P. (1998). Procedencia estratigráfica y edad de los más antiguos muroideos (Mammalia, Rodentia) de América del Sur. Ameghiniana 35: 473–475.Google Scholar
  50. Patterson, B., and Pascual, R. (1968). Evolution of mammals on southern continents. V. The fossil mammal fauna of South America. Q. Rev. Biol. 43: 409–451.Google Scholar
  51. Patterson, B., and Pascual, R. (1972). The fossil mammal fauna of South America. In: Evolution, Mammals, and Southern Continents, A. Keast, F. C. Erk, and B. Glass, eds., pp. 247–309, State University Press, Albany, NY.Google Scholar
  52. Patterson, B. D. (1992). A new genus and species of long-clawed mouse (Rodentia: Muridea) from temperate rainforests of Chile. Zool. J. Linn. Soc. 106: 127–145.Google Scholar
  53. Patterson, B. D., Gallardo, M. H., and Freas, K. E. (1984). Systematics of mice of the subgenus Akodon (Rodentia: Cricetidae) in southern South America, with the description of a new species. Fieldiana Zool. 23: 1–16.Google Scholar
  54. 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
  55. Patton, J. L., dos Reis, S. F., and da Silva, M. N. F. (1996). Relationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome B gene. J. Mammal. Evol. 3: 3–29.Google Scholar
  56. Pearson, O. P., and Patton, J. L. (1976). Relationships among South American phyllotine rodents based on chromosome analysis. J. Mammal. 57: 339–350.Google Scholar
  57. Pearson, O. P., and Smith, M. F. (1999). Genetic similarity between Akodon olivaceus and Akodon xanthorhinus (Rodentia, Muridae) in Argentina. J. Zool. Lond. 247: 43–52.Google Scholar
  58. Pine, R. H. (1973). Una nueva especie de Akodon (Mammalia: Rodentia: Muridae) de la Isla de Wellington, Magallanes, Chile. Anal. Inst. Patagonia 4: 423–426.Google Scholar
  59. Pine, R. H., Angle, J. P., and Bridge, D. (1978). Mammals from the sea, mainland and islands at the southern tip of South America. Mammalia 42: 105–114.Google Scholar
  60. Rambaut, A., and Bromham, L. (1998). Estimating divergence dates from molecular sequences. Mol. Biol. Evol. 15: 442–448.Google Scholar
  61. Reig, O. A. (1980). A new fossil genus of South American cricetid rodents allied to Wiedomys, with an assessment of the Sigmodontinae. J. Zool. Lond. 192: 257–281.Google Scholar
  62. Reig, O. A. (1984). Distribuição geográphica e história evolutiva dos roedores muroides sulamericanos (Cricetidae: Sigmodontinae). Revista Brasil. Genet. 7: 333–365.Google Scholar
  63. Reig, O. A. (1986). Diversity patterns and differentiation of high Andean rodents. In: High Altitude Tropical Biogeography, F. Vuilleumier and M. Monasterio, eds., pp. 404–439, Oxford University Press, London.Google Scholar
  64. Reig, O. A. (1987). An assessment of the systematics and evolution of the Akodontini, with the description of new fossil species of Akodon (Cricetidae: Sigmodontinae). Fieldiana Zool. 39: 347–399.Google Scholar
  65. Simpson, G. G. (1950). History of the fauna of Latin America. Am. Sci. 38: 361–389.Google Scholar
  66. Simpson, G. G. (1969). South American mammals. In: Biogeography and Ecology in South America, E. J. Fittkau et al., eds., pp. 879–909, D. W. Junk N.V., The Hague.Google Scholar
  67. Smith, M. F. (1998). Phylogenetic relationships and geographic structure in pocket gophers in the genus Thomomys. Mol. Phylogenet. Evol. 9: 1–14.Google Scholar
  68. 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.Google Scholar
  69. Smith, M. F., and Patton, J. L. (1993). The diversification of South American murid rodents: Evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol. J. Linn. Soc. 50: 149–177.Google Scholar
  70. Smith, M. F., Thomas, W. K., and Patton, J. L. (1992). Mitochondrial DNA-like sequence in the nuclear genome of an akodontine rodent. Mol. Biol. Evol. 9: 204–215.Google Scholar
  71. Spotorno, A. E. (1986). Systematics and Evolutionary Relationships of Andean Phyllotine and Akodontine Rodents, Unpublished Ph.D. thesis, University of California, Berkeley.Google Scholar
  72. Spotorno, A. E., Zuleta, C. A., and Cortes, A. (1990). Evolutionary systematics and heterochrony in Abrothrix species (Rodentia, Cricetidae). Evol. Biológica 4: 37–62.Google Scholar
  73. Steppan, S. J. (1993). Phylogenetic relationships among the Phyllotini (Rodentia: Sigmodontinae) using morphological characters. J. Mammal. Evol. 1: 187–213.Google Scholar
  74. 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
  75. Steppan, S. J., and Pardiñas, U. F. J. (1998). Two new fossil muroids (Sigmodontinae: Phyllotini) from the early Pleistocene of Argentina: phylogeny and paleoecology. J. Vert. Paleo. 18: 640–649.Google Scholar
  76. Sudman, P. D., and Hafner, M. S. (1992). Phylogenetic relationships among middle American pocket gophers (genus Orthogeomys) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 1: 17–25.Google Scholar
  77. Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sinauer Associates, Sunderland, MA.Google Scholar
  78. Swofford, D. L., Olsen, G. J., Waddell, P. J., and Hillis, D. M. (1996). Phylogenetic inference. In Molecular Systematics, D. M. Hills, C. Moritz, and B. K. Mable, eds., pp. 407–514, Sinauer Associates, Sunderland, MA.Google Scholar
  79. Tribe, C. J. (1996). The Neotropical Rodent Genus Rhipidomys (Cricetidae: Sigmodontinae)—a Taxonomic Revision, Unpublished Ph.D. thesis, University College London.Google Scholar
  80. Vorontzov, N. N. (1959). The system of hamster (Cricetinae) in the sphere of the world fauna and their phylogenetic relationships (in Russian). Biul. Moskovkogo Obshtschestea Ispitately Prirody Otdel Biol. 44: 134–137.Google Scholar
  81. Voss, R. S. (1988). Systematics and ecology of ichthyomyine rodents (Muroidea): Patterns of morphological evolution in a small adaptive radiation. Bull. Am. Mus. Nat. Hist. 188: 259–493.Google Scholar
  82. Voss, R. S. (1991a). On the identity of “Zygodontomys” punctulatus (Rodentia: Muroidea). Am. Mus. Novitates 3026: 1–8.Google Scholar
  83. Voss, R. S. (1991b). An introduction to the Neotropical muroid rodent genus Zygodontomys. Bull. Am. Mus. Nat. Hist. 210: 1–113.Google Scholar
  84. Voss, R. S. (1992). A revision of the South American species of Sigmodon (Mammalia: Muridae) with notes on their natural history and biogeography. Am. Mus. Novitates 3050: 1–56.Google Scholar
  85. Voss, R. S. (1993). A revision of the Brazilian muroid rodent genus Delomys with remarks on “thomasomyine” characters. Am. Mus. Novitates 3073: 1–44.Google Scholar
  86. Voss, R. S., and Carleton, M. D. (1993). A new genus for Hesperomys molitor Winge and Holochilus magnus Hershkovitz (Mammalia, Muridae) with an analysis of its phylogenetic relationships. Am. Mus. Novitates 3085: 1–39.Google Scholar
  87. Voss, R. S., and Linzey, A. V. (1981). Comparative gross morphology of male accessory glands among Neotropical Muridae (Mammalia: Rodentia) with comments on systematic implications. Misc. Publ. Mus. Zool. Univ. Mich. 159: 1–41.Google Scholar
  88. Webb, S. D. (1978). A history of savanna vertebrates in the New World. Part II: South America and the great interchange. Annu. Rev. Ecol. Syst. 9: 393–426.Google Scholar
  89. Webb, S. D. (1991). Ecogeography and the great American interchange. Paleobiology 17: 266–280.Google Scholar

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© Plenum Publishing Corporation 1999

Authors and Affiliations

  1. 1.Museum of Vertebrate ZoologyUniversity of CaliforniaBerkeley

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