Marsupials are viviparous, placental mammals that have evolved independently from the same ancestor as the eutherian mammals, which include humans and the principal laboratory animals. As a result of this evolutionary divergence, marsupial structure and function embody alternative solutions to many of the problems of mammalian existence. This dichotomy between marsupials and eutherian species suggests the use of marsupial models to provide innovative laboratory approaches that may facilitate experimental access to specific aspects of normal and abnormal human anatomy and physiology. Those characteristics that endow marsupials with their unique but largely unexploited biomedical research potential are identified and evaluated.
References
1.
1. Jurgelski, W., Jr. (1974). The opossum (Didelphis virginiana) as a biomedical model. I. Research perspective, husbandry and laboratory techniques. Lab. Anim. Sci.24, 375–403.
2.
2. Jurgelski, W. Jr. (1983). An alternative animal model for for perinatal carcinogenesis. Biol. Res. Preg.4, 3–16.
3.
3. Johnson, J.I. (1977). Central nervous system of marsupials. In: Biology of Marsupials.D. Hunsaker (ed.). New York: Academic Press, pp. 157–278.
4.
4. Clemens, W.A. (1977). Phylogeny of the marsupials. In: The Biology of Marsupials, B. Stonehouse and D. Gilmore (eds.). London: Macmillan, pp. 51–68.
5.
5. Tyndale-Biscoe, H. (1973). Life of Marsupials.New York: American Elsevier.
6.
6. Sharman, G.B. (1965). Marsupials and the evolution of viviparity. Viewpoints Biol.4, 1–28.
7.
7. Stonehouse, B. (1977). The marsupials. In: The Biology of Marsupials.B. Stonehouse and D. Gilmore (eds.). London: Macmillan, pp. 1–5.
8.
8. Renfree, M.B. (1981). Marsupials: alternative mammals. Nature293, 100–101.
9.
9. Hughes, R.L. (1974). Morphological studies on implantation in marsupials. J. Reprod. Fertil.39, 173–186.
10.
10. Fleming, M.W., and Harder, J.D. (1984). Uterine histology and reproductive cycles in pregnant and non-pregnant opossums, Didelphis virginiana. J. Reprod. Fert.62, 1–6.
11.
11. Taylor, J.M., and Padykula, H.A. (1978). Marsupial trophoblast and mammalian evolution. Nature271, 588.
12.
12. Kirsch, J.A.W. (1977). Biological aspects of the marsupial-placental dichotomy: A reply to Lillegraven. Evolution31, 898–900.
14. Kirsch, J.A.W. (1976). The classification of marsupials with special reference to karyotypes and serum proteins. In: The Biology of MarsupialsD. Hunsaker (ed.). New York: Academic Press, pp. 1–49.
15.
15. Simpson, G.G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist.85, 1–350.
16.
16. Kirsch, J.A.W., and Calaby, J.H. (1977). The species of living marsupials: an annotated text. In: The Biology of Marsupials.B. Stonehouse and D. Gilmore (eds.). London: Macmillan, pp. 9–26.
17.
17. Kirsch, J.A.W. (1977). The six percent solution: second thoughts on the adaption of Marsupialia. Am. Sci.65, 276–288.
18.
18. Barbour, R.A. (1977). Anatomy of marsupials. In: The Biology of Marsupials.B. Stonehouse and D. Gilmore (eds.). London: Macmillan, pp. 237–272.
19.
19. Wislocki, G.B., and Cambell, A.C.P. (1937). The unusual manner of vascularization of the brain of the opossum (Didelphis virginiana). Anat. Rec.67, 177–427.
20.
20. Scharrer, E. (1939). The regeneration of end arteries in the opossum brain. J. Comp. Neurol.70, 69–76.
21.
21. Scharrer, E. (1940). Further experiments on the regeneration of end arteries in the brain of the opossum. J. Exp. Zool.85, 365–381.
22.
22. Bubis, J.J., and Luce, S.A. (1964). An electron microscopic study of the cerebral blood vessels of the opossum. Zeitchr. Zellforsch.62, 16–25.
23.
23. Padykula, H.A., and Taylor, J.M. (1977). Uniqueness of the bandicoot chorio-allantoic placenta (Marsupialis: Peramelidae). Cytological and evolutionary interpretations. In: Reproduction and Evolution. Proc. of the Symposium on Comparative Biology of Reproduction.J. H. Calaby and C.H. Tyndale-Biscoe (eds.). Canberra: Aust. Acad. Sciences, pp. 303–323.
24.
24. Mccrady, E. Jr. (1938). The Embryology of the Opossum. Am. Anat. Mem. No. 16. Philadelphia: Wistar Institute of Anatomy and Biology.
25.
25. New, D.A.T., Mizell, M., and Cockroft, D.L. (1977). Growth of opossum embryos in vitro during organogenesis. J. Embryol. Exp. Morphol.41, 11–123.
26.
26. Renfree, M.B. (1970). Protein, amino acids, and glucose in the yolk-sac fluids and maternal blood sera of the tammar wallaby, Macropus eugenii. J. Reprod. Fertil.22, 483–92.
27.
27. Renfree, M.B. (1974). Yolk sac fluid and yolk sac membrane enzymes in the marsupial, Macropus eugenii. Comp. Biochem. Physiol.49B, 273.
28.
28. DeVRIES, P.A. (1978). Personal communication.
29.
29. Sadler, T.W. (1979). Culture of early somite mouse embryos during organogenesis. J. Embryol. Exp. Morpol.49, 17–25.
30.
30. New, D.A.T. (1978). Whole embryo culture and the study of mammalian embryos during organogenesis. Biol. Rev.53, 81–122.
31.
31. New, D.A.T. (1976). Personal communication.
32.
32. Kochbar, D.M. (1975). The use of in vitro procedures in teratology. Teratology11, 273–287.
33.
33. Godfrey, G.K. (1969). Reproduction in a laboratory colony of the marsupial mouse, Sminthopsis Iarapinta (Marsupialia: Dasyuridae). Aust. J. Zool.17, 637–654.
34.
34. Block, M. (1964). The blood-forming tissues and blood of the newborn opossum (Didelphis virginiana). I. Normal development through about the one hundredth day of life. Ergeb. Anat. Entwicklungsgesch.37, 327–366.
35.
35. Cutts, J.H., Krause, W.J., and Leeson, C.R. (1978). General observations on the growth and development of the young pouch opossum, Didelphis virginiana. Biol. Neonate33, 264–272.
36.
36. Blincoe, H. (1962). The structure of the non-motile hindlimb of the pouch young opossum. Anat. Rec.142, 89–93.
37.
37. Jurgelski, W. Jr., Hudson, P.M., and Falk, H.L. (1979). Tissue differentiation and susceptibility and embryonal tumor induction by ethyl nitrosourea in the opossum. In: Perinatal Carcinogenesis.J. M. Rice (ed). National Cancer Institute Monogram 51. Washington DC: US Dept. of Health Education and Welfare, pp. 123–158.
38.
38. Krause, W.J., Cutte, J.H., and Leeson, C.R. (1979). Morphological observations on the metanephros in the postnatal opossum, Didelphis virginiana. J. Anat.129, 377–397.
39.
39. Krause, W.J., Cutte, J.H., and Leeson, C.R. (1979). Morphological observations on the metanephros in the postnatal opossum, Didelphis virginiana. J. Anat.129, 459–477.
40.
40. Krause, W.J., and Leeson, C.R. (1973). Pre-and postnatal development of the respiratory system of the opossum. I. Light and scanning electron microscopy. Am. J. Anat.137, 337–356.
41.
41. Krause, W.J., and Leeson, C.R. (1975). Postnatal development of the respiratory system of the opossum. II. Electron microscopy of the epithelium and pleura. Acta Anat.92, 28–44.
42.
42. Burns, R.K. (1939). The differentiation of sex in the opossum (Didelphis virginiana) and its modification by the male hormone testosterone propionate. J. Morphol.65, 79–119.
43.
43. Hindes, R.D., and Mizell, M. (1976). The origin of immunoglobulins in opossum “embryos”. Dev. Biol.53, 49–61.
44.
44. Miller, P.A.F.J., Block, M., Rowlands, D.T. Jr., and Kind, P. (1965). Effect of thymectomy on hematopoietic organs of the opossum embryo. Proc. Soc. Exp. Biol. Med.118, 916–921.
45.
45. Rowlands, D.R., Jr., and Dudley, M.A. (1969). The development of serum proteins and humoral immunity in opossum embryos. Immunology17, 969–975.
46.
46. Bryant, B.J. (1977). The development of the lymphatic and immunohematopoietic systems. In: The Biology of Marsupials.D. Hunsaker (ed.). New York: Academic Press, pp. 349–385.
47.
47. Schield, J. (1966). Oxygen consumption during pouch development of the macropod marsupial, Setonix brachyurus. J. Physiol.187, 257–270.
48.
48. Reynolds, H.D. (1952). Studies on reproduction in the opossum, Didelphis virginiana. Univ. Calif. Publ. Zool.52, 223–284.
49.
49. Morrison, P., and Petajan, J.H. (1962). The development of temperature regulation in the opossum, Didelphis marsupialis Virginia. Physiol. Zool.35, 52–65.
50.
50. Sharman, G.B. (1973). Adaptations of marsupial pouch young for extrauterine existence. In: The Mammalian Fetus in Utero.C. R. Austin (ed.). London: Chapman-Hall, pp. 67–69.
51.
51. Bethlenfalvay, N.C., Block, M.H., and Brown, G.L. (1976). I. Hemoglobins of the opossum, Didelphis virginiana Kerr. Developmental changes from yolk sac to definitive erythropoiesis. Lab. Anim. Sci.26, 160–165.
52.
52. Burns, C.R. (1941). On the role of sex hormones in sex differentation in the opossum (Didelphis virginiana). Physiol. Zool.14, 1–45.
53.
53. Moore, C.R. (1943). Sexual differentiation in the opossum after early gonadectomy. J. Exp. Zool.94, 415–461.
54.
54. Burns, R.K. (1956). Hormones versus constitutional factors in the growth of embryonic sex primordia in the opossum. Am. J. Anat.98, 35–67.
55.
55. Morgan, C.F. (1943). The normal development of the ovary of the opossum from birth to maturity and its reactions to sex hormones. J. Morphol.72, 27–85.
56.
56. Setchell, P.J. (1974). The development of thermoregulation and thyroid function in the marsupial Macropus eugenii (Demarest). Comp. Biochem. Physiol.47A, 1115–1121.
57.
57. Lowrance, E.W. (1949). Variability and growth of the opossum skeleton. J. Morphol.85, 569–593.
58.
58. Washburn, S.L. (1946). The sequence of epiphyseal union in the opossum, Anat. Rec.95, 353–363.
59.
59. Nesslinger, C.L. (1956). Ossification centers and skeletal development in the postnatal Virginia opossum. J. Mammal37, 382–394.
60.
60. Farber, J.P., and Tenny, S.M. (1970). Development and ventilatory control mechanisms in the Virginia opossum. Physiologist13, 194.
61.
61. Farber, J.P., and Tenney, S.M. (1971). The pouch gas of the Virginia opossum (Didelphis virginiana). Resp. Physiol.11, 335–345.
62.
62. Farber, J.P., Hultgren, H.N., and Tenney, S.M. (1972). Development of the chemical control of breathing in the Virginia opossum. Resp. Physiol.14, 267–277.
63.
63. Farber, J.P. (1972). Development of pulmonary reflexes and pattern of breathing in the Virginia opossum. Resp. Physiol.15, 278–286.
64.
64. Larsell, O. (1935). Morphological and functional development of the membranous labyrinth in the opossum. J. Comp. Neurol.63, 95–118.
65.
65. Henkel, C.K., and Martin, G.F. (1977). The vestibular complex of the American opossum (Didelphis virginiana). I. Conformation, cytoarchitecture and primary vestibular imput. J. Comp. Neurol.172, 299–320.
66.
66. Henkel, C.K., and Martin, G.F. (1977). The vestibular complex of the American opossum (Didelphis virginiana). II. Afferent and efferent connections. J. Comp. Neurol.172, 321–348.
67.
67. Mcmanus, M.E., Mcgeachie, J.K., and Illett, K.F. (1978). Development of the hepatic mixed function oxidase system in a marsupial, quokka, Setonix brachyurus. Toxicol. Appl. Pharm.46, 117–124.
68.
68. Block, M. (1960). Wound healing in the newborn opossum, Didelphis virginiana. Nature187, 340–341.
69.
69. Clayson, D.B. (1981). Carcinogenesis in the developing organism: could protocols for testing be improved?. Biol. Res. Preg.2, 150–158.
70.
70. Carpenter, D.L., and Bitterly, J.G. (1965). Investigation of the specific and gross teratological effects of drugs on the development of the embryonic-fetal opossum, Report No. 25. Van Nuys, CA: The Marquardt Corporation.
71.
71. Barker, P.R., Bergman, H.C., Hunter, W.H., Lawrence, W.H., Steers, C.W., and Wright, L.N. (1967). Marsupial biomodule evaluation study. Document No. AMD-TR-66–3. Brooks, AFB, Texas: Aerospace Medical Division, Air Force Systems Command.
72.
72. Cadzow, N.G. (1974). Observations of Pouch Environment and Behavior of Pouch Young of the Virginia Opossum. Unpublished Thesis. Long Beach, California: California State University.
73.
73. Dawson, T.J., and Hulbert, A.J. (1969). Standard metabolism of marsupials. Nature221, 383.
74.
74. Macmillen, R.E., and Nelson, J.E. (1969). Bioenergetics and body size in dasyurid marsupials. Am. J. Physiol.217, 1246–1255.
75.
75. Katch, S., and Windsor, E. (1955). Unusual value for protein-bound iodine in the serum of the opossum. Science121, 897–898.
76.
76. Kinnear, J.E., and Brown, G.C. (1967). Minimum heart rates of marsupials. Nature215, 1501.
77.
77. Hayman, D.L. (1977). Chromosome number-constancy and variation. In: The Biology of Marsupials.B. Stonehouse and Gilmore, D. (eds.). London: Macmillan, pp. 27–48.
78.
78. Stonehouse, B., and Gilmore, D. (1977). The species and their chromosomes. In: The Biology of Marsupials.B. Stonehouse and D. Gilmore (eds). London: MacMillan, p. 7.
79.
79. Tyndale-Biscoe, C.H., Hearn, J.P., and Renfree, M.B. (1974). Control of reproduction in macropod marsupials. J. Endocrinol.63, 589–614.
80.
80. Tyndale-Biscoe, C.H. (1974). Reproduction in marsupials. J. Aust. Mamm. Soc.1, 175–180.
81.
81. Schneider, L.K. (1977). Marsupial chromosomes, cell cycles and cytogenetics. In: Biology of Marsupials. D. Hunsaker (ed.). New York: Academic Press, pp. 59–66.
82.
82. Buhl, S.N., Setlow, R.B., and Regan, J.D. (1974). DNA repair in Potorous tridactylus. Biophys. J.14, 791–803.
83.
83. Mortelmans, K., Cleaver, J.E., Friedberg, Paterson, M.C., Smith, B.P., and Thomas, G.H. (1977). Photoreactivation of thymine dimers in UV-irradiated human cells: unique dependence on culture conditions. Mutat. Res.44, 433–446.
84.
84. Hayman, D.L., and Martin, P.G. (1965). An autoradiographic study of DNA synthesis in the sex chromosome of two marsupials with an XX/XY1Y2 sex chromosome mechanism. Cytogenetics4, 209–218.
85.
85. Cooper, D.W. (1971). Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature230, 292–294.
86.
86. Kingbury, B.F. (1940). The development of the pharyngeal derivatives of the opossum, Didelphis virginiana, with special reference to the thymus. Am. J. Anat.67, 393–435.
87.
87. Biggers, J.D., and De Lamater, E.D. (1965). Marsupial spermatozoa pairing in the epididymis of American forms. Nature208, 402–404.
88.
88. Phillips, D.M. (1972). Comparative analysis of mammalian sperm motility. J. Cell Biol.53, 561–573.
89.
89. Bodian, D. (1951). Nerve endings, neurosecretory substance and lobular organization of the neurohypophysis. Johns Hopkins Hosp. Bull.89, 354–376.
90.
90. Zeballos, G.A., Wang, M.B., Kolzumi, K., and Brooks, C.M. (1967). Studies of the anterior hypothalamus of the opossum (Didelphis virginiana). Neuroendocrinology2, 88–98.
91.
91. Lende, R.A. (1936). Motor representation in the cerebral cortex of the opossum (Didelphis virginiana). J. Comp. Neurol.121, 405–415.
92.
92. Francq, E.N. (1969). Behavioral aspects of feigned death in the opossum (Didelphis marsupialis). Am. Midland Naturalist8, 556–567.
93.
93. Wiedorn, W.A. (1954). A new experimental animal for psychiatric research: The opossum, Didelphis virginiana. Science119, 360–361.
94.
94. Herring, F.H., Mason, D.J., Doolittle, J.H., and Starrett, D.E. (1966). The Virginia opossum in psychological research. Psychol. Rep.19, 755–757.
95.
95. Jurgelski, W., Hudson, P.M., and Vogel, F.S. (1973). Induction of a chronic somatosensory epilepsy in the opossum (Didelphis virginiana Kerr) with an inhibitor of cholesterol biosynthesis. Brain Res.64, 466–471.
96.
96. Kilmon, J.A. (1976). High tolerance to snake venom by the Virginia opossum, Didelphis virginiana. Toxicon14, 337–340.
97.
97. Werner, R.M., and Vick, J.A. (1977). Resistance of the opossum (Didelphis virginiana) to envenomation by snakes of the family Crotalidae. Toxicon15, 29–33.
98.
98. Winkelmann, R.F. (1964). Nerve endings of the North American opossum (Didelphis virginiana). A comparison with nerve endings of primates. Am. J. Phys. Anthropol.22, 253–258.
99.
99. Jurgelski, W. Jr., Hudson, P.M., Falk, H.L., and Kotin, P. (1976). Embryonal neoplasms in the opossum: A new model for solid tumors of infancy and childhood. Science193, 328–332.
100.
100. Jurgelski, W., Jr., Hudson, P.M., Falk, H.L., Zimmerman, L.E., Henry, J.M., and Palmer, N.F. (1978). Experimentally induced embryonal neoplasms in the opossum: Some aspects of tumor biology in comparison to analogous pediatric neoplasms in man. In: Tumors of Early Life in Man and Animals.L. Sevier (ed.). Monteluce, Italy: Perugia Quadrenial International Conference on Cancer, pp. 1087–1109.
101.
101. Jurgelski, W., Jr., Hudson, P.M., Dunn, R.L., and Falk, H.L. (1977). A new animal model for the direct induction of neoplasms during embryonic and fetal development. In: Proc. Third Int. Symp. on Detection and Prevention of Cancer, Part I. H. E. Nieburgs (ed.). New York: Marcel Decker, pp. 1033–1059.
102.
102. Willis, R.A. (1962). The Borderline of Embryology and Pathology, 2nd ed.London: Butterworths.
103.
103. Christensen, J., and Lund, G.F. (1969). Esophageal responses to distension and electrical stimulation. J. Clin. Invest.48, 408–419.
104.
104. Schulze, K., Dodds, W.J., Christensen, J., and Wood, J.D. (1977). Esophageal manometry in the opossum. Am. J. Physiol.233, E152–159.
105.
105. Laplante, E.S., and Burrell, R.G. (1966). Bacterial endocarditis in opossums. Bull. Wildlife Dis. Assoc.2, 10–12.
106.
106. Sherwood, B.F., Rowlands, F.T., Vakilzadek, J., and Lemay, J.C. (1971). Experimental bacterial endocarditis in the opossum (Didelphis virginiana). Am. J. Pathol.64, 513–520.
107.
107. Meneghini, R. (1974). Repair replication of opossum lymphocyte DNA: effect of compounds that bind to DNA. Chem. Biol. Interact.8, 113–126.
108.
108. Martin, P.G. (1965). The potentialities of the fat-tailed marsupial mouse Sminthopsis crassicaudata (Gould) as a laboratory animal. Aust. J. Zool.13, 559–562.
