The Mammary Gland and Its Origin During Synapsid Evolution

  • Olav T. Oftedal


Lactation appears to be an ancient reproductive trait that predates the origin of mammals. The synapsid branch of the amniote tree that separated from other taxa in the Pennsylvanian (>310 million years ago) evolved a glandular rather than scaled integument. Repeated radiations of synapsids produced a gradual accrual of mammalian features. The mammary gland apparently derives from an ancestral apocrine-like gland that was associated with hair follicles. This association is retained by monotreme mammary glands and is evident as vestigial mammary hair during early ontogenetic development of marsupials. The dense cluster of mammo-pilo-sebaceous units that open onto a nipple-less mammary patch in monotremes may reflect a structure that evolved to provide moisture and other constituents to permeable eggs. Mammary patch secretions were coopted to provide nutrients to hatchlings, but some constituents including lactose may have been secreted by ancestral apocrine-like glands in early synapsids. Advanced Triassic therapsids, such as cynodonts, almost certainly secreted complex, nutrient-rich milk, allowing a progressive decline in egg size and an increasingly altricial state of the young at hatching. This is indicated by the very small body size, presence of epipubic bones, and limited tooth replacement in advanced cynodonts and early mammaliaforms. Nipples that arose from the mammary patch rendered mammary hairs obsolete, while placental structures have allowed lactation to be truncated in living eutherians.

mammary gland cutaneous gland evolution Synapsida monotreme marsupial 


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  1. 1.
    W. K. Gregory (1910). The orders of mammals. Bull.Am.Mus. Nat.Hist.27: 1–524.Google Scholar
  2. 2.
    D. G. Blackburn, L. J. Vit, and C. A. Beuchat (1984). Eutherian-like reproductive specializations in a viviparous reptile. Proc.Natl.Acad.Sci.U.S.A.81: 4860–4863.Google Scholar
  3. 3.
    D. G. Blackburn (1992). Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Am.Zool.32: 313–321.Google Scholar
  4. 4.
    L. Fishelson and A. Baranes (1998). Observations on the Oman shark, Iago omanensis (Triakidae), with emphasis on the morphological and cytological changes of the oviduct and yolk sac during gestation. J.Morphol.236: 151–165.Google Scholar
  5. 5.
    M. H. Wake (1993). Evolution of oviductal gestation in amphibians. J.Exp.Zool. 266: 394–413.Google Scholar
  6. 6.
    J. P. Wourms (1981). Viviparity: The maternal-fetal relationship in fishes. Am.Zool.21: 473–515.Google Scholar
  7. 7.
    D. G. Blackburn, V. Hayssen, and C. J. Murphy (1989). The origin of lactation and the evolution of milk: A review with new hypotheses. Mammal Rev.19: 1–26.Google Scholar
  8. 8.
    O. T. Oftedal (2002). The origin of lactation as a water source for parchment-shelled eggs. J.Mammary Gland Biol. Neoplasia 7: 253–266.PubMedGoogle Scholar
  9. 9.
    C. Darwin (1859). On the Origin of Species by Means of Nat-ural Selection, or the Preservation of Favoured Races in the Struggle of Life, John Murray, London.Google Scholar
  10. 10.
    St. G. Mivart (1871). On the Genesis of Species, D. Appleton, New York.Google Scholar
  11. 11.
    C. Darwin (1872). On the Origin of Species by Means of Nat-ural Selection, 6th edn., Appleton-Century-Crofts, New York.Google Scholar
  12. 12.
    R. Owen (1832). On the mammary glands of the Or-nithorhynchus paradoxus.Philos.Trans.R.Soc.Lond. 1832: 517–538.Google Scholar
  13. 13.
    A. Moyal (2001). Platypus: The Extraordinary Story of how a Curious Creature Baffled the World, Smithsonian Institution Press, Washington, DC.Google Scholar
  14. 14.
    M. Griffiths (1978). Biology of the Monotremes, Academic Press, New York.Google Scholar
  15. 15.
    C. Gegenbauer (1886). Zur Kenntniss der Mammarorgane der Monotremen, W. Engelmann, Leipzig, Germany.Google Scholar
  16. 16.
    E. Bresslau (1907). Die Entwickelung des Mammarappa-rates der Monotremen, Marsupialier und einiger Placentalier. I. Entwickelung und Ursprung des Mammarapparates von Echidna. Jenaische Denkschr.7: 459–518, Plates 28–30. [Un-dated, but cited as 1907 in Ref. 18].Google Scholar
  17. 17.
    E. Bresslau (1912). Die Entwickelung des Mammarapparates der Monotremen, Marsupialer und einiger Placentalier. III. Entwickelung des Mammarapparates der Marsupialer, Insec-tivoren, Nagathiere, Carnivoren und Wiederkaeuer. Jenaische Denkschr.7: 647–874, Plates 37–46. [Undated, but cited as 1912 in introductory note to Ref. 18]Google Scholar
  18. 18.
    E. Bresslau (1920). The Mammary Apparatus of the Mam-malia in Light of Ontogenesis and Phylogenesis, Methuen, London.Google Scholar
  19. 19.
    J. B. S. Haldane (1964). The origin of lactation. Rationalist Ann. 1964: 19–30.Google Scholar
  20. 20.
    J. B. S. Haldane (1965). The possible evolution of lactation. Zool.Jb.Syst.92: 41–48.Google Scholar
  21. 21.
    C. A. Long (1969). The origin and evolution of mammary glands. Bioscience 19: 519–523.Google Scholar
  22. 22.
    C. A. Long (1972). Two hypotheses on the origin of lactation. Am.Nat. 106: 141–144.Google Scholar
  23. 23.
    J. A. Hopson (1973). Endothermy, small size, and the origin of mammalian reproduction. Am.Nat. 107: 446–452.Google Scholar
  24. 24.
    B. M. Graves and D. Duvall (1983). A role of aggregation pheromones in the evolution of mammallike reptile lactation. Am.Nat. 122: 835–839.Google Scholar
  25. 25.
    D. Duvall (1986). A new question of pheromones: Aspects of chemical signaling and reception in the mammal-like reptiles. In N. Hotton, P. D. MacLean, J. J. Roth, and E. C. Roth (eds.), The Ecology and Biology of Mammal-Like Reptiles, Smithsonian Institution Press, Washington, DC, pp. 219–238.Google Scholar
  26. 26.
    V. Hayssen and D. G. Blackburn (1985). α-lactalbumin and the origins of lactation. Evolution 39: 1147–1149.Google Scholar
  27. 27.
    L. J. Guillette and N. Hotton (1986). The evolution of mammalian reproductive characteristics in therapsid reptiles. In N. Hotton, P. D. MacLean, J. J. Roth, and E. C. Roth (eds.), The Ecology and Biology of Mammal-Like Reptiles, Smithsonian Institution Press, Washington, DC, pp. 239–250.Google Scholar
  28. 28.
    D. G. Blackburn (1991). Evolutionary origins of the mammary gland. Mammal Rev. 21: 81–98.Google Scholar
  29. 29.
    Q. Ji, Z.-X. Luo, C.-X. Yuan, J. R. Wible, J.-P. Zhang, and J. A. Georgi (2002). The earliest known eutherian mammal. Nature 416: 816–822.PubMedGoogle Scholar
  30. 30.
    T. S. Kemp (1982). Mammal-Like Reptiles and the Origin of Mammals, Academic Press, London.Google Scholar
  31. 31.
    M. J. Benton (1997). Vertebrate Paleontology, 2nd edn., Chapman & Hall, London.Google Scholar
  32. 32.
    M. J. Packard and R. S. Seymour (1997). Evolution of the amniote egg. In S. S. Sumida and K. L. M. Martin (eds.), Amniote Origins: Completing the Transition to Land, Academic Press, San Diego, CA, pp. 265–290.Google Scholar
  33. 33.
    A. S. Romer and L. W. E. Price (1940). Review of the Pely-cosauria. Geol.Soc.Am.Spec.Pap. 28: 1–538.Google Scholar
  34. 34.
    J. A. Hopson (1994). Synapsid evolution and the radiation of non-eutherian mammals. In D. B. Prothero and R. M. Schoch (eds.), Major Features of Vertebrate Evolution, Paleontological Society, Knoxville, TN, pp. 190–219.Google Scholar
  35. 35.
    F. S. Szalay (1994). Evolutionary History of the Marsupials and an Analysis of Osteological Characters, Cambridge University Press, Cambridge, UK.Google Scholar
  36. 36.
    C. A. Sidor and J. A. Hopson (1998). Ghost lineages and “mammalness”: Assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24: 254–273.Google Scholar
  37. 37.
    Z.-X. Luo, A. W. Crompton, and A.-L. Sun (2001). A new mammaliaform from the early Jurassic and evolution of mammalian characteristics. Science 292: 1535–1540.PubMedGoogle Scholar
  38. 38.
    N. Hotton, P. D. MacLean, J. J. Roth, and E. C. Roth (eds.) (1986). The Ecology and Biology of Mammal-Like Reptiles, Smithsonian Institution Press, Washington, DC.Google Scholar
  39. 39.
    C. G. Farmer (2000). Parental care: The key to understanding endothermy and other convergent features in birds and mammals. Am.Nat. 155: 326–334.PubMedGoogle Scholar
  40. 40.
    T. S. Kemp (1983). The relationships of mammals. Zool.J. Linn.Soc.77: 353–384.Google Scholar
  41. 41.
    B. S. Rubidge and C. A. Sidor (2001). Evolutionary pat-terns among Permo-Triassic therapsids. Ann.Rev.Ecol.Syst. 32: 449–480.Google Scholar
  42. 42.
    E. Mayr (2001). What Evolution Is, Basic Books, New York.Google Scholar
  43. 43.
    D. H. Erwin (1993). The Great Paleozoic Crisis: Life and Death in the Permian, Columbian University Press, New York.Google Scholar
  44. 44.
    Z.-X. Luo, R. L. Cifelli, and Z. Kielan-Jaworowska (2001). Dual origin of tribosphenic mammals. Nature 409: 53–57.PubMedGoogle Scholar
  45. 45.
    D. S. Berman, S. S. Sumida, and R. E. Lombard (1997). Bio-geography of primitive amniotes. In S. S. Sumida and K. L. M. Martin (eds.), Amniote Origins: Completing the Transition to Land, Academic Press, San Diego, CA, pp. 85–139.Google Scholar
  46. 46.
    R. L. Carroll (1988). Vertebrate Paleontology and Evolution, W. H. Freeman, New York.Google Scholar
  47. 47.
    P. Michaelson (2002). Mass extinction of peat-forming plants and the effect on fluvial styles across the Permian–Triassic boundary, northern Bowen Basin, Australia. Palaeogeogr. Palaeoclimatol.Palaeoecol. 179: 173–188.Google Scholar
  48. 48.
    G. King (1990). The Dicynodonts: A Study in Palaeobiology, Chapman and Hall, London.Google Scholar
  49. 49.
    A. Chinsamy and B. S. Rubidge (1993). Dicynodont (Therap-sida) bone histology: Phylogenetic and physiological implications. Palaeont.Afr. 30: 97–102.Google Scholar
  50. 50.
    J. Botha and A. Chinsamy (2000). Growth patterns deduced from the bone histology of the cynodonts Diademodon and Cynognathus. J.Vert.Paleont. 20: 705–711.Google Scholar
  51. 51.
    W. Maier, J. van den Heever, and F. Durand (1996). New ther-apsid specimens and the origin of the secondary hard and soft palate of mammals. J.Zool.Syst.Evol.Res.34: 9–19.Google Scholar
  52. 52.
    W. J. Hillenius (1994). Turbinates in therapsids: Evidence for late Permian origins of mammalian endothermy. Evolution 48: 207–229.Google Scholar
  53. 53.
    J. Ruben (1995). The evolution of endothermy in mammals and birds: From physiology to fossils. Ann.Rev.Physiol. 57: 69–95.Google Scholar
  54. 54.
    A. W. Crompton, C. R. Taylor, and J. A. Jagger (1978). Evolution of homeothermy in mammals. Nature 272: 333–336.PubMedGoogle Scholar
  55. 55.
    M. Griffiths, M. A. Elliott, R. M. C. Leckie, and G. I. Schoefl (1973). Observations of the comparative anatomy and ultra-structure of mammary glands and on the fatty acids of the triglycerides in platypus and echidna milk fats. J.Zool.Lond. 169: 255–279.Google Scholar
  56. 56.
    M. Griffiths (1983). Lactation in Monotremata and speculations concerning the nature of lactation in Cretaceous Multi-tuberculata. Palaeont.Polonica 28: 93–102.Google Scholar
  57. 57.
    T. D. White (1989). An analysis of epipubic bone function in mammals using scaling theory. J.Theor.Biol. 138: 343–357.Google Scholar
  58. 58.
    M. J. Novacek, G. W. Rougier, J. R. Wible, M. C. McKenna, D. Dashzeveg, and I. Horovitz (1997). Epipubic bones in eu-therian mammals from the Late Cretaceous of Mongolia. Na-ture 389: 483–486.Google Scholar
  59. 59.
    J. A. Lillegraven (1979). Reproduction in Mesozoic mam-mals. In J. A. Lillegraven, Z. Kielan-Jaworowska, and W. A. Clemens (eds.), Mesozoic Mammals: The First Two-Thirds of Mammalian History, University of California Press, Berkeley, CA, pp. 259–276.Google Scholar
  60. 60.
    Y. Hu, Y. Wang, Z. Luo, and C. Li (1997). Anewsymmetrodont mammal from China and its implications for mammalian evo-lution. Nature 390: 137–142.PubMedGoogle Scholar
  61. 61.
    J. Qiang, L. Zhexi, and J. Shu-an (1999). A Chinese tricon-odont mammal and mosaic evolution of the mammalian skele-ton. Nature 398: 326–330.PubMedGoogle Scholar
  62. 62.
    K. A. Kermack (1956). Tooth replacement in mammal-like reptiles of the suborders Gorgonopsia and Therocephalia. Philos.Trans.R.Soc.Lond.B 670: 95–133.Google Scholar
  63. 63.
    A. W. Crompton and Z. Luo (1993). Relationships of the Lias-sic mammals Sinoconodon, Morganucodon oehleri, and Din-netherium. In F. S. Szalay, M. J. Novacek, and M. C. McKenna (eds.), Mammal Phylogeny: Mesozoic Differentiation, Mul-tituberculates, Monotremes, Early Therians, and Marsupials, Springer-Verlag, New York, pp. 30–44.Google Scholar
  64. 64.
    C. M. Pond (1977). The significance of lactation in the evolution of mammals. Evolution 31: 177–199.Google Scholar
  65. 65.
    J. Kear and N. Duplaix-Hall (eds.) (1975). Flamingos,T&AD Poyser, Berkhamstead, England.Google Scholar
  66. 66.
    S. Shetty, L. Bharathi, K. B. Shenoy, and S. N. Hegde (1992). Biochemical properties of pigeon milk and its effect on growth. J.Comp.Physiol.B 162: 632–636.Google Scholar
  67. 67.
    N. D. Horseman and J. D. Buntin (1995). Regulation of pigeon cropmilk secretion and parental behaviors by prolactin. Ann. Rev.Nutr. 15: 213–238.Google Scholar
  68. 68.
    O. T. Oftedal (1984). Milk composition, milk yield and energy output at peak lactation: A comparative review. Symp.Zool. Soc.Lond.51: 33–85.Google Scholar
  69. 69.
    B. Green and J. C. Merchant (1988). The composition of mar-supial milk. In C. H. Tyndale-Biscoe and P. A. Janssens (eds.), The Developing Marsupial.Models for Biomedical Research, Springer-Verlag, Berlin, pp. 41–54.Google Scholar
  70. 70.
    L. M. Frolich (1997). The role of the skin in the origin of am-niotes: Permeability barrier, protective covering and mechan-ical support. In S. S. Sumida and K. L. M. Martin (eds.), Am-niote Origins: Completing the Transition to Land, Academic Press, San Diego, CA, pp. 327–352.Google Scholar
  71. 71.
    H. B. Lillywhite and P. F. A. Maderson (1982). Skin structure and permeability. In C. Gans and F. H. Pough (eds.), Biology of the Reptilia, Vol.12: Physiology C: Physiological Ecology, Academic Press, New York, pp. 397–442.Google Scholar
  72. 72.
    R. I. C. Spearman (1973). The Integument: ATextbook of Skin Biology, Cambridge University Press, Cambridge, England.Google Scholar
  73. 73.
    W. E. Duellman and L. Trueb (1994). Biology of Amphibians, Johns Hopkins University Press, Baltimore.Google Scholar
  74. 74.
    G. Delfino, R. Brizzi, R. Kracke-Berndorff, and B. Alvarez (1998). Serous gland dimorphism in the skin of Melanophryniscus stelzneri(Anura: Bufonidae). J.Morphol. 237: 19–32.PubMedGoogle Scholar
  75. 75.
    B. T. Clarke (1997). The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biol.Rev. 72: 365–379.PubMedGoogle Scholar
  76. 76.
    L. P. Fredericks and J. R. Dankert (2000). Antibacterial and hemolytic activity of the skin of the terrestrial salamander, Plethodon cinereus.J.Exp.Zool. 287: 340–345.Google Scholar
  77. 77.
    W. A. Buttemer (1990). Effect of temperature on evapora-tive water loss of the Australian tree frogs Litoria caerula and Litoria chloris. Physiol.Zool. 63: 1043–1057.Google Scholar
  78. 78.
    L. A. Blaylock, R. Ruibal, and K. Platt-Aloia (1976). Skin structure and wiping behavior of Phyllomedusine frogs. Copeia 1976: 283–295.Google Scholar
  79. 79.
    P. F. A. Madderson, T. Rabinowitz, B. Tandler, and L. Alibardi (1998). Ultrastructural contributions to an understanding of the cellular mechanisms involved in lizard skin shedding with comments on the function and evolution of a unique lepi-dosaurian phenomenon. J.Morphol. 236: 1–24.Google Scholar
  80. 80.
    P. D. Oldak (1976). Comparison of the scent gland secretion lipids of twenty-five snakes: Implications for biochemical sys-tematics. Copeia 1976: 320–326.Google Scholar
  81. 81.
    W. B. Quay (1986). The skin of reptiles: Glands. In J. Bereiter-Hahn, A. G. Matoltsy, and K. S. Richards (eds.), Biology of the Integument, Vol.2: Vertebrates, Springer-Verlag, Berlin, pp. 188–193.Google Scholar
  82. 82.
    R. O. Prum (1999). Development and evolutionary origin of feathers.J.Exp.Zool. 285: 291–306.PubMedGoogle Scholar
  83. 83.
    P. R. Stettenheim (2000). The integumentary morphology of modern birds—An overview. Am.Zool. 40: 461–477.Google Scholar
  84. 84.
    V. R. Wheatley (1986). The Physiology and Pathophysiology of the Skin, Vol.9: The Sebaceous Glands, Academic Press, London.Google Scholar
  85. 85.
    R. I. C. Spearman (1977). Hair follicle development, cyclical changes and hair form. In A. Jarrett (ed.), The Physiology and Pathophysiology of the Skin, Vol.4: The Hair Follicle, Academic Press, London, pp. 1255–1292.Google Scholar
  86. 86.
    S. A. Czerkas (1997). Skin. In P. J. Currie and K. Padian (eds.), Encyclopedia of Dinosaurs, Academic Press, San Diego, CA, pp. 669–675.Google Scholar
  87. 87.
    P. K. Chudinov (1968). Structure of the integuments of theromorphs. Dokl.Acad.Sci.U.S.S.R.Earth Sci.Sect.179: 226–229.Google Scholar
  88. 88.
    M. B. L. Craigmyle (1984). The Apocrine Glands and the Breast, Wiley, Chichester, England.Google Scholar
  89. 89.
    H. J. Harlow (1984). The influence of Hardarian gland removal and fur lipid removal on heat loss and water flux to and from the skin of muskrats, Ondatra zibethicus. Physiol.Zool. 57: 349–356.Google Scholar
  90. 90.
    W. Montagna and R. A. Ellis (1960). Sweat glands in the skin of Ornithorhynchus paradoxus. Anat.Rec. 137: 271–277.PubMedGoogle Scholar
  91. 91.
    W. Montagna and P. F. Parakkal (1974). The Structure and Function of Skin, 3rd edn., Academic Press, New York.Google Scholar
  92. 92.
    B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter (2002). Molecular Biology of the Cell, 4th edn., Garland Science, New York.Google Scholar
  93. 93.
    F. B. P. Wooding (1980). Lipid droplet secretion by the rabbit Harderian gland. J.Ultrastruct.Res. 71: 68–78.PubMedGoogle Scholar
  94. 94.
    A. Raynaud (1961). Morphogenesis of the mammary gland. In S. K. Kon and A. T. Cowie (eds.), Milk: The Mammary Gland and Its Secretion, Vol.1, Academic Press, New York, pp. 3–46.Google Scholar
  95. 95.
    G. W. Robinson, A. B. C. Karpf, and K. Kratochwil (1999). Regulation of mammary gland development by tissue inter-action. J.Mammary Gland Biol.Neoplasia 4: 9–19.PubMedGoogle Scholar
  96. 96.
    A. T. Cowie and J. S. Tyndal (1971). The Physiology of Lacta-tion, Edward Arnold London.Google Scholar
  97. 97.
    H. Tyndale-Biscoe and M. Renfree (1987). Reproductive Physiology of Marsupials, Cambridge University Press, Cam-bridge, UK.Google Scholar
  98. 98.
    A. J. Thody and S. Shuster (1989). Control and function of sebaceous glands. Physiol.Rev. 69: 383–416.PubMedGoogle Scholar
  99. 99.
    L. Requena, H. Kiryu, and A. B. Ackerman (1998). Neo-plasms With Apocrine Differentiation, Lippincott-Raven, Philadelphia.Google Scholar
  100. 100.
    R. Wrench, J. A. Hardy, and R. I. C. Spearman (1980). Se-bokeratocytes of avian epidermis—with mammalian compar-isons. In R. I. C. Spearman and P. A. Riley (eds.), The Skin of Vertebrates, Academic Press, London, pp. 47–55.Google Scholar
  101. 101.
    A. M. W. Porter (2001). Why do we have apocrine and seba-ceous glands? J.R. Soc.Med.94: 236–237.PubMedGoogle Scholar
  102. 102.
    M. C. Neville, D. Medina, J. Monks, and R. C. Hovey (1998). Editorial commentary: The mammary fat pad. J.Mammary Gland Biol.Neoplasia 3: 109–116.PubMedGoogle Scholar
  103. 103.
    G. R. Buzell (1996). The Harderian gland: Perspectives. Microsc.Res.Tech.34: 2–5.PubMedGoogle Scholar
  104. 104.
    Y. Seyama, H. Otsuka, K. Ohashi, B. Vivien-Roels, and P. Pevet (1996). Sexual diversity of the lipid metabolism in the Harderian gland of the golden hamster. Microsc.Res.Tech. 34: 71–76.PubMedGoogle Scholar
  105. 105.
    I. H. Mather and T. W. Keenan (1998). Origin and secretion of milk lipids. J.Mammary Gland Biol.Neoplasia 3: 259–273.PubMedGoogle Scholar
  106. 106.
    M. M. T. Janssen and P. Walstra (1982). Cytoplasmic remnants in milk of certain species. Neth.Milk Dairy J. 36: 365–368.Google Scholar
  107. 107.
    S. J. Gould (1977). Ontogeny and Phylogeny, Harvard University Press, Cambridge, MA.Google Scholar
  108. 108.
    E. Mayr (1994). Recapitulation reinterpreted: The somatic program. Q.Rev.Biol.64: 223–232.Google Scholar
  109. 109.
    S. F. Gilbert and J. A. Bolker (2001). Homologies of process and modular elements of embryonic construction. J.Exp. Zool. 291: 1–12.PubMedGoogle Scholar
  110. 110.
    G. Mayer and M. Klein (1961). Histology and cytology of the mammary gland. In S. K. Kon and A. C. Cowie (eds.), Milk: The Mammary Gland and Its Secretion, Academic Press, New York, pp. 47–126.Google Scholar
  111. 111.
    M. Griffiths (1968). Echidnas, Pergamon Press, Oxford, Eng-land.Google Scholar
  112. 112.
    M. Griffiths, D. L. McIntosh, and R. E. A. Coles (1969). The mammary gland of the echidna, Tachyglossus aculeatus, with observations on the incubation of the egg and on the newly-hatched young. J.Zool.Lond. 158: 371–386.Google Scholar
  113. 113.
    M. Griffiths, D. L. McIntosh, and R. M. C. Leckie (1972). The mammary glands of the red kangaroo with observations on the fatty acid components of the milk triglycerides. J.Zool. Lond. 166: 265–275.Google Scholar
  114. 114.
    P. Viacava, A. G. Naccarato, and G. Bevilacqua (1997). Apoc-rine epithelium of the breast: Does it result from metaplasia? Virchows Arch.431: 205–209.PubMedGoogle Scholar
  115. 115.
    T. Sakakura (1987). Mammary embryogenesis. In M. C. Neville and C. W. Daniel (eds.), The Mammary Gland: De-velopment, Regulation, and Function, Plenum, New York, pp. 36–66.Google Scholar
  116. 116.
    M. M. Richert, K. L. Schwertfeger, J. W. Ryder, and S. M. Anderson (2000). An atlas of mouse mammary gland devel-opment. J.Mammary Gland Biol.Neoplasia 5: 227–241.PubMedGoogle Scholar
  117. 117.
    B. A. Howard and B. A. Gusterson (2000). Human breast development. J.Mammary Gland Biol.Neoplasia 5: 119–137.PubMedGoogle Scholar
  118. 118.
    P. A. Masso-Welch, K. M. Darcy, N. C. Stangle-Castor, and M. M. Ip (2000). Adevelopmental atlas of rat mammary gland histology. J.Mammary Gland Biol.Neoplasia 5: 165–185.PubMedGoogle Scholar
  119. 119.
    W. Montagna (1962). The Structure and Function of Skin, 2nd edn., Academic Press, New York.Google Scholar
  120. 120.
    T. L. Taigen, F. H. Pough, and M. M. Stewart (1984). Water balance of terrestrial anuran (Eleutherodactylus coqui) eggs: Importance of parental care. Ecology 65: 248–255.Google Scholar
  121. 121.
    R. A. Nussbaum (1985). The evolution of parental care in salamanders. Misc.Publ.Mus.Zool.Univ.Mich.(No. 169), pp. 1–50.Google Scholar
  122. 122.
    Anonymous (1999). Legless amphibians nurse their young. Science 283: 623.Google Scholar
  123. 123.
    J. P. Hill (1933). The development of the Monotremata. Part II. The structure of the eggshell. Trans.Zool.Soc.Lond.21: 443–477.Google Scholar
  124. 124.
    H. Burrell (1974). The Platypus, Rigby, Adelaide, Australia.Google Scholar
  125. 125.
    J. P. Hill (1949). Development of the Monotremata. Part VII. The development and structure of the egg-tooth and the caruncle in the monotremes and on the occurrence of vestiges of the egg-tooth and caruncle in marsupials. Trans.Zool.Soc. Lond.26: 503–544.Google Scholar
  126. 126.
    H. B. White (1991). Maternal diet, maternal proteins and egg quality. In D. C. Deeming and M. W. J. Ferguson (eds.), Egg In-cubation: Its Effects on Embryonic Development in Birds and Reptiles, Cambridge University Press, Cambridge, England, pp. 1–15.Google Scholar
  127. 127.
    D. S. Newburg (1996). Oligosaccharides and glycoconjugates in human milk: Their role in host defense. J.Mammary Gland Biol.Neoplasia 1: 271–283.PubMedGoogle Scholar
  128. 128.
    T. Urashima, T. Saito, T. Nakamura, and M. Messer (2001). Oligosaccharides of milk and colostrum in non-human mam-mals. Glycoconj.J.18: 357–371.PubMedGoogle Scholar
  129. 129.
    M. Messer and T. Urashima (2002). Evolution of milk oligosac-charides and lactose. Trends Glycosci.Glycotechnol.14: 153–176.Google Scholar
  130. 130.
    M. Charron, J. H. Shaper, and N. L. Shaper (1998). The increased level of ¯1,4-galactosyltransferase required for lactose biosynthesis is achieved in part by translational control. Proc.Natl.Acad.Sci.U.S.A.95: 14805–14810.PubMedGoogle Scholar
  131. 131.
    N. L. Shaper, M. Charron, N.-W. Lo, and J. H. Shaper (1998). ¯1,4-Galactosyltransferase and lactose biosynthesis: Recruitment of a housekeeping gene from the nonmammalian ver-tebrate gene pool for a mammary gland specific function. J. Mammary Gland Biol.Neoplasia 3: 315–324.PubMedGoogle Scholar
  132. 132.
    C. P. Piotte, C. J. Marshall, M. J. Hubbard, C. Collet, and M. R. Grigor (1997). Lysozyme and α-lactalbumin from the milk of a marsupial, the common brush-tailed possum (Trichosurus vulpecula). Biochim.Biophys.Acta 1336: 235–242.PubMedGoogle Scholar
  133. 133.
    J. L. Linzell and M. Peaker (1971). Mechanism of milk secre-tion. Physiol.Rev. 51: 564–597.PubMedGoogle Scholar
  134. 134.
    M. J. Packard and N. B. Clark (1996). Aspects of calcium regulation in embryonic lepidosaurians and chelonians and a review of calcium regulation in embryonic archosaurians. Phys-iol. Zool. 69: 435–466.Google Scholar
  135. 135.
    J. R. Stewart and M. B. Thompson (2000). Evolution of placen-tation among squamate reptiles: Recent research and future directions. Comp.Biochem.Physiol.A 127: 411–431.Google Scholar
  136. 136.
    M. R. Ginger and M. R. Grigor (1999). Comparative aspects of milk caseins. Comp.Biochem.Physiol.B 124: 133–145.PubMedGoogle Scholar
  137. 137.
    B. Green, K. Newgrain, and J. Merchant (1980). Changes in milk composition during lactation in the tammar wallaby (Macropus eugenii). Aust.J.Biol.Sci. 33: 35–42.PubMedGoogle Scholar
  138. 138.
    E. A. Crisp, P. E. Cowan, and M. Messer (1989). Changes in milk carbohydrates during lactation in the common brushtail possum, Trichosurus vulpecula(Marsupialia: Phalangeridae). Reprod.Dom.Anim.1: 309–314.Google Scholar
  139. 139.
    E. A. Crisp, M. Messer, and J. L. VandeBerg (1989). Changes in milk carbohydrates during lactation in a didelphid marsupial, Monodelphis domestica. Physiol.Zool. 62: 1117–1125.Google Scholar
  140. 140.
    B. Green, J. L. VandeBerg, and K. Newgrain (1991). Milk com-position in an American marsupial (Monodelphis domestica). Comp.Biochem.Physiol.B 99: 663–665.PubMedGoogle Scholar
  141. 141.
    B. Green, W. J. Krause, and K. Newgrain (1996). Milk compo-sition in the North American opossum (Didelphis virginiana). Comp.Biochem.Physiol.B 113: 619–623.PubMedGoogle Scholar
  142. 142.
    M. Messer and K. R. Nicholas (1991). Biosynthesis of marsupial milk oligosaccharides: Characterization and developmental changes of two galactosyltransferases in lactating mammary glands of the tammar wal-laby, Macropus eugenii.Biochim.Biophys.Acta 1077: 79–85.Google Scholar
  143. 143.
    T. Urashima, M. Messer, and W. A. Bubb (1992). Biosynthesis of marsupial milk oligosaccharides II: Characterization of a ¯6-N-acetylglucosaminyltransferase in lactating mammary glands of the tammar wallaby, Macropus eugenii. Biochim. Biophys.Acta 1117: 223–231.PubMedGoogle Scholar
  144. 144.
    O. T. Oftedal (1980). Milk and mammalian evolution. In K. Schmidt-Nielsen, L. Bolis, and C. R. Taylor (eds.), Compar-ative Physiology: Primitive Mammals, Cambridge University Press, Cambridge, pp. 31–42.Google Scholar
  145. 145.
    R. L. Hughes and L. S. Hall (1988). Structural adaptations of the newborn marsupial. In C. H. Tyndale-Biscoe and P. A. Janssens (eds.), The Developing Marsupial: Models for Biomedical Research, Springer-Verlag, Berlin, pp. 8–27.Google Scholar
  146. 146.
    R. L. Hughes (1993). Monotreme development with particular reference to the extraembryonic membranes. J.Exp.Zool. 266: 480–494.PubMedGoogle Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Olav T. Oftedal
    • 1
  1. 1.Department of Conservation BiologyConservation and Research Center, Smithsonian National Zoological ParkWashington, District of Columbia

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