Advertisement

Journal of Mammalian Evolution

, Volume 7, Issue 1, pp 43–77 | Cite as

Phylogenetic Studies on Didelphid Marsupials I. Introduction and Preliminary Results from Nuclear IRBP Gene Sequences

  • Sharon A. Jansa
  • Robert S. Voss
Article

Abstract

We report and analyze nucleotide sequence variation in the first exon (1158 bp) of the nuclear gene encoding the Interphotoreceptor Retinoid Binding Protein (IRBP) among 21 species representing all 15 currently recognized genera of living didelphids. Six previously published IRBP sequences representing five nondidelphimorph marsupial orders were also analyzed to test didelphid monophyly, and 12 published sequences representing ten placental orders were used as outgroups. No gaps (indels) are necessary to align didelphid sequences, but one short region (35 bp) is alignment-ambiguous among nondidelphids. Uncorrected pairwise sequence divergence ranges from 0.7 to 5.7% among nonconspecific didelphids, from 9.2 to 15.3% between didelphids and nondidelphid marsupials, and from 24.9 to 32.1% between marsupials and placentals. Neither transitions nor transversions exhibit saturation for any codon position at any level of taxonomic comparison. Parsimony analyses of these data provide strong support (bootstrap values >95%, Bremer values ≥7) for the monophyly of (1) Didelphidae ("caluromyines" + Didelphinae); (2) a group containing Caluromys and Caluromysiops; (3) Didelphinae; (4) a group of large opossums that includes Metachirus; (5) a group containing the remaining large opossums (with 2N = 22 chromosomes); (6) a group containing Marmosa and Micoureus; (7) a group containing Thylamys, Lestodelphys, and Gracilinanus; and (8) a group containing the last three genera plus a monophyletic Marmosops. In addition, we found moderate support (bootstrap values >80%, Bremer values ≥2) for the monophyly of Thylamys + Lestodelphys and for a sister-group relationship between Monodelphis and Marmosa + Micoureus. Sensitivity analysis suggests that all of these clades, together with their associated levels of bootstrap and Bremer support, are robust to alternative hypotheses of positional homology within the ambiguously alignable region. Although some of the relationships supported by IRBP are not consistent with the results of published morphological analyses, our reassessment of the morphological data suggests that many conflicts are more apparent than real.

marsupials IRBP Didelphidae phylogeny mammalian systematics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

LITERATURE CITED

  1. Anderson, S. (1997). Mammals of Bolivia, taxonomy and distribution. Bull. Amer. Mus. Nat. Hist. 231: 1–652.Google Scholar
  2. Aplin, K. P., and Archer, M. (1987). Recent advances in marsupial systematics with a new syncretic classification. In: Possums and Opossums: Studies in Evolution, M. Archer, ed., pp. xv–lxii. Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  3. Archer, M. (1976). The basicranial region of marsupicarnivores (Marsupialia), interrelationships of carnivorous marsupials, and affinities of the insectivorous marsupial peramelids. Zool. J. Linn. Soc. 59: 217–322.Google Scholar
  4. Atramentowicz, M. (1986). Dynamique de population chez trois marsupiaux didelphid´es de Guyane. Biotropica 18: 136–149.Google Scholar
  5. Bensley, B. A. (1903). On the evolution of the Australian Marsupialia; with remarks on the relationships of the marsupials in general. Trans. Linn. Soc. London (Zool.) Ser. 2 9: 83–217.Google Scholar
  6. Biggers, J. D., and DeLamater, E. D. (1965). Marsupial spermatozoa pairing in the epididymis of American forms. Nature 208: 402–404.Google Scholar
  7. Boardman, W. (1951). The hair tracts of some American marsupials. Proc. Linn. Soc. London 121: 845–850.Google Scholar
  8. Bremer, K. (1994). Branch support and tree stability. Cladistics 6: 369–372.Google Scholar
  9. Bridges, C. D. B., Liou, G. I., Alvarez, R. A., Landers, R. A., Landry, A. M., Jr., and Fong, S.-L. (1986). Distribution of interstitial retinol-binding protein (IRBP) in the vertebrates. J. Exp. Zool. 239: 335–346.Google Scholar
  10. Charles-Dominique, P. (1983). Ecology and social adaptations in didelphids marsupials: comparisons with eutherians of similar ecology. In: Advances in the Study of Mammalian Behavior, J. F. Eisenberg and D. G. Kleiman, eds., pp. 395–422, Spec. Publ. 7, Amer. Soc. Mammal.Google Scholar
  11. Clemens, W. A. (1968). Origin and early evolution of marsupials. Evolution 22: 1–18.Google Scholar
  12. Clemens, W. A. (1977). Phylogeny of the marsupials. In: The Biology of Marsupials, B. Stonehouse and D. Gilmore, eds., pp. 51–68. University Park Press, Baltimore, MD.Google Scholar
  13. Colgan, D. J. (1999). Phylogenetic studies of marsupials based on phosphoglycerate kinase DNA sequences. Mol. Phylogeny Evol. 11: 13–26.Google Scholar
  14. Creighton, G. K. (1984). Systematic Studies on Opossums (Didelphidae) and Rodents (Cricetidae). Ph.D. Diss., Univ. Michigan. Univ. Microfilms International, Ann Arbor, MI.Google Scholar
  15. DeSalle, R., and Brower, A. V. Z. (1999). Process partition, congruence, and the independence of characters: Inferring relationships among closely related Hawaiian Drosophila from multiple gene regions. System. Biol. 46: 751–764.Google Scholar
  16. DeSalle, R., Wray, C., and Absher, R. (1994). Computational problems in molecular systematics. In: Molecular Ecology and Evolution: Approaches and Applications, B. Schierwater, B. Streit, G. P. Wagner, and R. DeSalle, eds., pp. 353–370, Birkhauser Verlag, Basel, Switzerland.Google Scholar
  17. Dollo, L. (1899). Les ancestres des marsupiaux etaient-ils arboricoles? Trav. Stat. Zool. Wimereus 7: 188–203.Google Scholar
  18. Eernisse, D. J., and Kluge, A. G. (1993). Taxonomic congruence versus total evidence, and amniote phylogeny inferred from fossils, molecules, and morphology. Mol. Biol. Evol. 10: 1170–1195.Google Scholar
  19. Engstrom, M. D., and Gardner, A. L. (1988). Karyotype of Marmosa canescens (Marsupialia: Didelphidae): a mouse opossum with 22 chromosomes. Southwest. Nat. 33: 231–233.Google Scholar
  20. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.Google Scholar
  21. Fong, S.-L., and Bridges, C. D. B. (1988). Internal quadruplication in the structure of human interstitial retinolbinding protein deduced from its cloned cDNA. J. Biol. Chem. 263: 15330–15334.Google Scholar
  22. Fong, S.-L., Fong, W.-B., Morris, T. A., Kedzie, K. M., and Bridges, C. D. B. (1990). Characterization and comparative structural features of the gene for human interstitial retinol-binding protein. J. Biol. Chem. 265: 3648–3653.Google Scholar
  23. Gardner, A. L. (1993). Didelphimorphia. In: Mammal Species of the World: A Taxonomic and Geographic Reference, D. E. Wilson and D. M. Reeder, eds., pp. 15–23, Smithsonian Institution Press, Washington, D.C.Google Scholar
  24. Gardner, A. L., and Creighton, G. K. (1989). A new generic name for Tate's (1933) Microtarsus group of South American mouse opossums (Marsupialia: Didelphidae). Proc. Biol. Soc. Washington 102: 3–7.Google Scholar
  25. Gatesy, J., DeSalle, R., and Wheeler, W. (1993). Alignment-ambiguous nucleotide sites and the exclusion of systematic data. Mol. Phylogeny Evol. 2: 152–157.Google Scholar
  26. Gatesy, J., Milinkovitch, M., Waddell, V., and Stanhope, M. (1999). Stability of cladistic relationships between Cetacea and higher-level artiodactyl taxa. System. Biol. 48: 6–20.Google Scholar
  27. Gemmell, N. J., and Westerman, M. (1994). Phylogenetic relationships within the class Mammalia: A study using mitochondrial 12S RNA sequences. J. Mammal. Evol. 2: 3–23.Google Scholar
  28. Goin, F. J. (1993). Living South American opossums are not living fossils. In: Abstracts of Spoken and Poster Papers, Sixth International Theriological Congress, Sydney, Australia, M. L. Augee, ed., p. 112.Google Scholar
  29. Goin, F. J., and Rey, P. (1997). Sobre las afinidades de Monodelphis Burnett, 1830 (Mammalia: Marsupialia: Didelphidae: Marmosinae). Neotr´opica 43: 93–98.Google Scholar
  30. Grand, T. I. (1983). Body weight: its relationship to tissue composition, segmental distribution of mass, and motor function III. The Didelphidae of French Guyana. Aust. J. Zool. 31: 299–312.Google Scholar
  31. Gregory, W. K. (1910). The orders of mammals. Bull. Amer. Mus. Nat. Hist. 27: 1–524.Google Scholar
  32. Harder, J. D. (1992). Reproductive biology of South American marsupials. In: Reproductive Biology of South American Vertebrates, W. C. Hamlett, ed., pp. 211–228, Springer-Verlag, New York.Google Scholar
  33. Hershkovitz, P. (1992). The South American gracile mouse opossums, genus Gracilinanus Gardner and Creighton, 1989 (Marmosidae, Marsupialia): a taxonomic review with notes on general morphology and relationships. Fieldiana Zool. [NS] 70: 1–56.Google Scholar
  34. Hill, J. P., and Fraser, E. A. (1925). Some observations on the female urogenital organs of the Didelphydae. Proc. Zool. Soc. London 1925: 189–219.Google Scholar
  35. Huxley, T. H. (1880). On the application of the laws of evolution to the arrangement of the Vertebrata and more particularly of the Mammalia. Proc. Zool. Soc. London 1880: 649–662.Google Scholar
  36. Kirsch, J. A. W. (1977). The comparative serology of the Marsupialia, and a classification of marsupials. Aust. J. Zool. Suppl. Ser. 52: 1–152.Google Scholar
  37. Kirsch, J. A. W., and Archer, M. (1982). Polythetic cladistics, or, when parsimony's not enough: the relationships of carnivorous marsupials. In: Carnivorous Marsupials, M. Archer, ed., pp. 595–619. Roy. Zool. Soc. NSW, Mosman, Australia.Google Scholar
  38. Kirsch, J. A. W., and R. E. Palma (1995). DNA/DNA hybridization studies of carnivorous marsupials. V. A further estimate of relationship among opossums (Marsupialia: Didelphidae). Mammalia 59: 403–425.Google Scholar
  39. Kirsch, J. A. W., Dickerman, A. W., and Reig, O. A. (1995). DNA/DNA hybridization studies of carnivorous marsupials IV. Intergeneric relationships of the opossums (Didelphidae). Marmosiana 1: 57–78.Google Scholar
  40. Kirsch, J. A. W., Lapointe, F.-J., and M. S. Springer. (1997) DNA-hybridization studies of marsupials and their implications for metatherian classification. Aust. J. Zool. 45: 211–280.Google Scholar
  41. Kluge, A. G., and Wolf, A. J. (1993). Cladistics: What's in a word? Cladistics 9: 136–199.Google Scholar
  42. Lemelin, P. (1999). Morphological correlates of substrate use in didelphid marsupials: Implications for primate origins. J. Zool. London 247: 165–175.Google Scholar
  43. Lockhart, P. J., Howe, C. J., Bryany, D. A., Benaland, T. J., and Larkum, A. W. D. (1992). Substitutional bias confounds inference of cyanelle origins from sequence data. J. Mol. Evol. 34: 153–162.Google Scholar
  44. Luckett, W. P. (1994). Suprafamilial relationships within Marsupialia: Resolution and discordance from multidisciplinary data. J. Mammal. Evol. 2: 255–283.Google Scholar
  45. Lyne, A. G. (1959). The systematic and adaptive significance of the vibrissae in the Marsupialia. Proc. Zool. Soc. London 133: 79–133.Google Scholar
  46. Maddison, W. P., and Maddison, D. R. (1992). MacClade, Version 3.06. Sinauer, Sunderland, MA.Google Scholar
  47. Marshall, L. G. (1979). Evolution of metatherian and eutherian (mammalian) characters: a review based on cladistic methodology. Zool. J. Linn. Soc. London 66: 369–410.Google Scholar
  48. Marshall, L. G., Case, J. A., and Woodburne, M. O. (1990). Phylogenetic relationships of the families of marsupials. Current Mammal. 2: 433–505.Google Scholar
  49. Marshall, L. G., Muizon, C., and Sigogneau-Russell, D. (1995). Pucadelphys andinus (Marsupialia, Mammalia) from the early Paleocene of Bolivia. Mem. Mus. Nat. Hist. Natur. 165: 1–164.Google Scholar
  50. McNab, B. K. (1978). The comparative energetics of Neotropical marsupials. J. Comp. Physiol. 125: 115–128.Google Scholar
  51. Moore, H. D. M. (1996). Gamete biology of the New World marsupial, the grey short-tailed opossum, Monodelphis domestica. Reprod. Fertil. Develop. 8: 605–615.Google Scholar
  52. Mustrangi, M. A., and Patton, J. L. (1997). Phylogeography and systematics of the slender mouse opossum Marmosops (Marsupialia, Didelphidae). Univ. Calif. Publ. Zool. 130: 1–86.Google Scholar
  53. Nixon, K. C., and Carpenter, J. M. (1996). On simultaneous analysis. Cladistics 12: 305–321.Google Scholar
  54. Nogueira, J. C., Silva, M. N. F., and Câmara, B. G. O. (1999). Morphology of the male genital system of the bushy-tailed opossum Glironia venusta Thomas, 1912 (Didelphimorphia, Didelphidae). Mammalia 63: 231–236.Google Scholar
  55. Osgood, W. H. (1921). A monographic study of the American marsupial Caenolestes, with a description of the brain of Caenolestes by C. Judson Herrick. Field Mus. Nat. Hist. Zool. Ser. 14(1): 1–162.Google Scholar
  56. Patton, J. L., and Silva, M. N. F. (1997). Definition of species of pouched four-eyed opossums (Didelphidae, Philander). J. Mammal. 78: 90–102.Google Scholar
  57. Patton, J. L., dos Reis, S. F., and 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
  58. Patton, J. L., da Silva, M. N. F., and Malcolm, J. R. (2000). Mammals of the Rio Juru´a and the evolutionary and ecological diversification of Amazonia. Bull. Am. Mus. Nat. Hist. 244: 1–306.Google Scholar
  59. Pepperberg, D. R., Okajima, T.-I. L., Wiggert, B., Ripps, H., Crouch, R. K., and Chader, G. J. (1993). Interphotoreceptor Retinoid Binding Protein (IRBP): Molecular biology and physiological role in the visual cycle of rhodopsin. Mol. Neurobiol. 7: 61–84.Google Scholar
  60. Reig, O. A. (1955). Noticia preliminar sobre la presencia de microbiotherinos vivientes en la fauna sudamericana. Invest. Zool. Chil. 2: 121–130.Google Scholar
  61. Reig, O. A., Gardner, A. L., Bianchi, N. O., and Patton, J. L. (1977). The chromosomes of the Didelphidae (Marsupialia) and their evolutionary significance. Biol. J. Linn. Soc. London 9: 191–216.Google Scholar
  62. Reig, O. A., Kirsch, J. A. W., and 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: Possums and Opossums: Studies in Evolution, M. Archer, ed., pp. 1–89, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  63. Retief, J. D., Krajewski, C., Westerman, M., Winkfein, R. J., and Dixon, G. H. (1995). Molecular phylogeny and evolution of marsupial protamine P1 genes. Proc. Roy. Soc. London B 259: 7–14.Google Scholar
  64. Rougier, G. W., Wible, J. R., and Novacek, M. J. (1998). Implications of Deltatheridium specimens for early marsupial history. Nature 396: 459–463.Google Scholar
  65. Saccone, C., Pesole, G., and Preparata, G. (1989). DNA microenvironments and the molecular clock. J. Mol. Evol. 29: 407–411.Google Scholar
  66. Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Amer. Mus. Nat. Hist. 85: 1–350.Google Scholar
  67. Sonntag, C. F. (1924). The comparative anatomy of the tongues of the Mammalia. XI. Marsupialia and Montotremata. Proc. Zool. Soc. London 49: 743–755.Google Scholar
  68. Sorenson, M. (1996). TreeRot. University of Michigan, Ann Arbor, MI.Google Scholar
  69. Springer, M. S., Westerman, M., and Kirsch, J. A. W. (1994). Relationships among orders and families of marsupials based on 12S ribosomal DNA sequences and the timing of the marsupial radiation. J. Mammal. Evol. 2: 85–115.Google Scholar
  70. Springer, M. S., Burk, A., Kavanagh, J. R., Waddell, V. G., and Stanhope, M. J. (1997a). The interphotoreceptor retinoid binding protein gene in therian mammals: Implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc. Natl. Acad. Sci. U.S.A. 94: 13754–13759.Google Scholar
  71. Springer, M. S., Kirsch, J. A. W., and Case, J. A. (1997b). The chronicle of marsupial evolution. In: Molecular Evolution and Adaptive Radiation, T. J. Givnish and K. J. Sytsma, eds., pp. 129–161, Cambridge University Press, Cambridge.Google Scholar
  72. Springer, M. S., Amrine, H. M., Burk, A., and Stanhope, M. J. (1999). Additional support for Afrotheria and Paenungulata, the performance of mitochondrial versus nuclear genes, and the impact of data partitions with heterogeneous base composition. System. Biol. 48: 65–75.Google Scholar
  73. Stanhope, M. J., Czelusniak, J., Si, J.-S., Nickerson, J., and Goodman, M. (1992). A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. Mol. Phylogeny Evol. 1: 148–160.Google Scholar
  74. Stanhope, M. J., Smith, M. R., Waddell, V. G., Porter, C. A., Shivji, M. S., and Goodman, M. (1996). Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: Convincing evidence for several superordinal clades. J. Mol. Evol. 43: 83–92.Google Scholar
  75. Szalay, F. S. (1982a). A new appraisal of marsupial phylogeny and classification. In: Carnivorous Marsupials, M. Archer, ed., pp. 621–640, Roy. Zool. Soc. NSW, Mosman, Australia.Google Scholar
  76. Szalay, F. S. (1982b). Phylogenetic relationships of the marsupials. Geobios Mem. Spec. 6: 177–190.Google Scholar
  77. Szalay, F. S. (1994). Evolutionary History of the Marsupials and an Analysis of Osteological Characters. Cambridge Univ. Press, New York.Google Scholar
  78. Tate, G. H. H. (1933). A systematic revision of the marsupial genus Marmosa, with a discussion of the adaptive radiation of the murine opossums. Bull. Amer. Mus. Nat. Hist. 46: 1–250.Google Scholar
  79. Tate, G. H. H. (1947). Results of the Archibold Expeditions. No. 56: On the anatomy and classification of the Dasyuridae (Marsupialia). Amer. Mus. Nat. Hist. 88: 97–156.Google Scholar
  80. Temple-Smith, P. (1987). Sperm structure and marsupial phylogeny. In: Possums and Opossums: Studies in Evolution, M. Archer, ed., pp. 171–193, Surrey Beatty & Sons, Chipping Norton, Australia.Google Scholar
  81. Temple-Smith, P. D., and Bedford, J. M. (1980). Sperm maturation and the formation of sperm pairs in the epididymis of the opossum, Didelphis virginiana. J. Exp. Zool. 214: 161–171.Google Scholar
  82. Thompson, J. D., Higgins, D. G., and 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 Res. 22: 4673–4680.Google Scholar
  83. Wheeler, W. C. (1995). Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. System. Biol. 44: 321–331.Google Scholar
  84. Wible, J. R. (1990). Petrosals of late Cretaceous marsupials from North America, and a cladistic analysis of the petrosal in therian mammals. J. Vert. Paleontol. 10: 183–205.Google Scholar
  85. Winge, H. (1893). Jordfundne og nulevende Pungdyr (Marsupialia) fra Lagoa Santa, Minas Geraes, Brasilien. E Museo Lundii 2(2): 1–132.Google Scholar
  86. Wroe, S. (1997). A reexamination of proposed morphology-based synapomorphies for the families of Dasyuromorphia (Marsupialia). I. Dasyuridae. J. Mammal. Evol. 4: 19–52.Google Scholar
  87. Yates, T. L., Jones, C., and Cook, J. A. (1996). Preservation of voucher specimens. In: Measuring and Monitoring Biological Diversity, Standard Methods for Mammals, D. E. Wilson, F. R. Cole, J. D. Nichols, R. Rudran, and M. S. Foster, eds., pp. 265–273, Smithsonian Institution Press, Washington, D.C. and London.Google Scholar
  88. Yoder, A. D., and Irwin, J. A. (1999). Phylogeny of the Lemuridae: Effects of character and taxon sampling on resolution of species relationships within Eulemur. Cladistics 15: 351–361.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Sharon A. Jansa
    • 1
  • Robert S. Voss
    • 2
  1. 1.Department of MammalogyAmerican Museum of Natural HistoryNew York
  2. 2.Department of MammalogyAmerican Museum of Natural HistoryNew York

Personalised recommendations