Comparative patterns of craniofacial development in eutherian and metatherian mammals

Evolution

Volumn 51, Issue 5, 1997, Pages 1663-1678

  Smith, Kathleen K ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Development; Evolution; Heterochrony; Mammals; Marsupial; Placental

Indexed keywords

EUTHERIA; MAMMALIA; METATHERIA;

EID: 0030828084     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1997.tb01489.x     Document Type: Article

References (113)

1. ALBERCH, P. 1985. Problems with the interpretation of developmental sequences. Syst. Zool. 34:46-58.
2. ALBERCH, P., S. J. GOULD, G. F. OSTER, AND D. B. WAKE. 1979. Size and shape in ontogeny and phylogeny. Paleobiology 5:296-317.
3. ATCHLEY, W. R., AND B. K. HALL. 1991. A model for development and evolution of complex morphological structures. Biol. Rev. 66:101-157.
4. BRIDGE, D. T., AND D. ALLBROOK. 1970. Growth of striated muscle in an Australian marsupial (Setonix brachyurus). J. Anat. 106: 285-295.
5. BUTLER, H., AND B. J. J. JUURLINK. 1987. An atlas for staging mammalian and chick embryos. CRC Press, Boca Raton, FL.
6. CARROLL, R. L. 1988. Vertebrate paleontology and evolution. Freeman, New York.
7. CHEEK, D. B. 1975. Fetal and postnatal cellular growth. Wiley, New York.
8. CLARK, C. T. 1990. A comparative study of cranial skeletal ontogeny in two marsupials, Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). Ph.D. diss. Duke Univ., Durham. NC.
9. CLARK, C. T., AND K. K. SMITH. 1993. Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J. Morph. 215:1 19-149.
10. COCKBURN, A. 1989. Adaptive patterns in marsupial reproduction. Trends Ecol. Evol. 4:126-130.
11. CUBBAGE, C. C., AND P. M. MABEE. 1996. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J. Morph. 229:121-160.
12. DHOPESHWARKAR, G. A. 1983. Nutrition and brain development. Plenum Press, New York.
13. DOBBING, J. 1972. Vulnerable periods in brain development. Pp. 9-20 in K. Elliot and J. Knight, eds. Lipids, malnutrition and the developing brain. Ciba Foundation Symposium. Vol. 3. Elsevier, Amsterdam, The Netherlands.
14. DODGE, P. R., A. L. PRENSKY, AND R. D. FEIGIN. 1975. Nutrition and the developing nervous system. Mosby Co., Saint Louis, MO.
15. DUNLOP, L.-L. T., AND B. K. HALL. 1995. Relationships between cellular condensation, preosteoblast formation and epithelial-mesenchymal interactions in initiation of osteogenesis. Int. J. Devel. Bio. 39:357-371.
16. EISENBERG, J. R. 1981. The mammalian radiations. Univ. of Chicago Press, Chicago.
17. ESDAILE, P. C. 1916. On the structure and development of the skull and laryngeal cartilages of Perameles with notes on the cranial nerves. Phil. Trans. R. Soc., Ser. B Biol. Sci. 207:439-479.
18. FILAN, S. L. 1991. Development of the middle ear region in Monodelphis domestica (Marsupialia, Didelphidae): marsupial solutions to early birth. J. Zool., Lond. 225:577-588.
19. FRIGO, L., AND P. A. WOOLLEY. 1996. Development of the skeleton of the stripe-faced Dunnart, Sminthopsis macroura (Marsupialia: Dasyuridae). Aust. J. Zool. 44:155-164.
20. GEMMELL, R. T., AND J. NELSON. 1988. Ultrastructure of the ol-factory system of three newborn marsupial species. Anat. Rec. 221:655-662.
21. _. 1992. Development of the vestibular and auditory system of the northern native cat, Dasyurus hallucatus. Anat. Rec. 234: 136-143.
22. GEMMELL, R. T., AND L. SELWOOD. 1994. Structural development in the newborn marsupial, the stripe-faced dunnart, Sminthopsis macroura. Acta Anat. 149:1-12.
23. GEMMELL, R. T., G. JOHNSTON, AND M. M. BRYDEN. 1988. Osteogenesis in two marsupial species, the bandicoot Isoodon macrourus and the possum Trichosurus vulpecula. J. Anat. 159:155-164.
24. GRIBNAU, A. A. M., AND L. G. M. GEIJBERTS. 1981. Developmental stages in the Rhesus monkey (Macaco mulatto). Adv. Anat., Emb. Cell Bio. 68:1-84.
25. GRÜNEBERG, H. 1963. The pathology of development. Wiley, New York.
26. HALL, B. K. 1984. Genetic and epigenetic control of connective tissues in the craniofacial structures. Birth Defects: Original Article Series 20:1-17.
27. _. 1987. Tissue interactions in the development and evolution of the vertebrate head. Pp. 215-259 in P. F. A. Maderson. ed. Developmental and evolutionary aspects of the neural crest. Wiley-Interscience. New York.
28. _. 1991. Cellular interactions during cartilage and bone development. J. Craniofac. Genet. Devel. Bio. 11:238-250.
29. HALL, B. K., AND S. W. HERRING. 1990. Paralysis and growth of the musculoskeletal system in the embryonic chick. J. Morph. 206:45-56.
30. HALL, B. K., AND T. MIYAKE. 1992. The membranous skeleton: the role of cell condensations in vertebrate skeletogenesis. Anat. Embry. 186:107-124.
31. HALL, L. S., AND R. L. HUGHES. 1987. An evolutionary perspective of structural adaptations for environmental perception and utilization by the neonatal marsupials Trichosurus vulpecula (Phalangeridae) and Didelphis virginiana (Didelphidae). Pp. 257-271 in M. Archer, ed. Possums and opossums: studies in evolution. Surrey Beatty and Sons, Sydney.
32. HANKEN, J. 1983. Miniaturization and its effects on cranial morphology in Plethodontid salamanders, genus Thorius (Amphibia: Plethodontidae). II. The fate of the brain and sense organs and their role in skull morphogenesis and evolution. J. Morph. 177: 255-268.
33. HANKEN, J., AND P. THOROGOOD. 1993. Evolution and development of the vertebrate skull: the role of pattern formation. Trends Ecol. Evol. 8:9-15.
34. HARTMAN, C G. 1919. Studies on the development of the opossum (Didelphis virginiana L.). J. Morph. 32:1-144.
35. HAYSSEN, V., R. C. LACY, AND P. J. PARKER. 1985. Metatherian reproduction: transitional or transcending? Am. Nat. 126:617-632.
36. HERRING, S. W. 1993a. Epigenetic and functional influences on skull growth. Pp. 153-206 in J. Hanken and B. K. Hall, eds. The skull. Vol. 1. Univ. of Chicago Press, Chicago.
37. _. 1993b. Formation of the vertebrate face: epigenetic and functional influences. Am. Zool. 33:472-483.
38. HERSCHKOWITZ, N. 1989. Brain development and nutrition. Pp. 297-304 in P. Evrard and A. Minkowski, eds. Developmental neurobiology. Vevey/Raven Press, New York.
39. HETZEL, B. S., AND R. M. SMITH. 1981. Fetal brain disorders. Elsevier/North Holland, Amsterdam, The Netherlands.
40. HILL, J. P., AND W. C. O. HILL. 1955. The growth stages of the pouch young of the native cat (Dasyurus viverrinus) together with observations on the anatomy of the newborn young. Trans. Zool. Soc., Lond. 28:349-453.
41. HOLT, A. B., M. B. RENFREE, AND D. B. CHEEK. 1981. Comparative aspects of brain growth: a critical evaluation of mammalian species used in brain growth research with emphasis on the Tammar wallaby. Pp. 17-43 in B. S. Hetzel, and R. M. Smith, eds. Fetal brain disorders - recent approaches to the problem of mental deficiency. Elsevier/North-Holland, Amsterdam, The Netherlands.
42. HUGHES, R. L., AND L. S. HALL. 1984. Embryonic development in the common brushtail possum. Trichosurus vulpecula. Pp. 197-212 in A. P. Smith and I. D. Hume eds. Possums and gliders. Australian Mammal Society, Sydney.
43. _. 1988. Structural adaptations of the newborn marsupial. Pp. 8-27 in C. H. Tyndale-Biscoe and P. A. Janssens. eds. The developing marsupial. Models for biomedical research. Springer, Berlin.
44. HUISMAN, F. J. 1933. Tabellarische uebersicht der Entwicklung von Manis javanica Desm. A. Oosthoek, Utrecht.
45. KIRSCH, J. A. W. 1977a. Biological aspects of the marsupial-placental dichotomy: a reply to Lillegraven. Evolution 31:898-900.
46. _. 1977b. The six-percent solution: second thoughts on the adaptedness of the Marsupialia. Am. Sci. 65:276-288.
47. -. 1977c. The comparative serology of Marsupialia, and a classification of marsupials. Aust. J. Zool., Suppl. 52:1-152.
48. KLIMA, M. 1987. Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Springer, Berlin.
49. KRAUSE, W. J., AND N. R. SALINDERS. 1994. Brain growth and neocortical development in the opossum. Ann. Anat. 176:395-407.
50. LANGE, D. DE., AND H. F. NIERSTRASZ. 1932. Tabellarische uebersicht der Entwicklung von Tupaia javanica Horsf. A. Oosthoek, Utrecht.
51. LEE, A. K., AND A. COCKBURN. 1985. Evolutionary ecology of marsupials. Cambridge Univ. Press, Cambridge.
52. LILLEGRAVEN, J. A. 1975. Biological considerations of the marsupial-placental dichotomy. Evolution 29:707-722.
53. . 1979. Reproduction in Mesozoic mammals. Pp. 259-276 in J. A. Lillegraven, Z. Kielan-Jaworowska, and W. A. Clemens, eds. Mesozoic mammals. Univ. of California Press, Berkeley.
54. _. 1984. Why was there a "marsupial-placental dichotomy?" Pp. 72-86 in P. D. Gingerich and C. E. Badgley, eds. Mammals: notes for a short course. University of Tennessee studies in geology 8. Univ. of Tennessee, Knoxville.
55. LILLEGRAVEN, J. A., S. D. THOMPSON, B. K. MCNAB, AND J. L. PATTON. 1987. The origin of eutherian mammals. Biol. J. Linn. Soc. 32:281-336.
56. LUCKETT, W. P. 1994. Suprafamilial relationships within Marsupialia: resolution and discordance from multidisciplinary data. J. Mamm. Evol. 2:255-283.
57. MABEE, P. M. 1993. Phylogenetic interpretation of ontogenetic change: sorting out the actual and artifactual in an empirical case study of centrarchid fishes. Zool. J. Linn. Soc. 107:175-291.
58. MABEE, P. M., AND T. A. TRENDLER. 1996. Development of the cranium and paired fins in Betta splendens (Teleostei: Percomorpha): intraspecific variation and interspecific comparisons. J. Morph. 227:249-287.
59. MADDISON, W. P., AND D. R. MADDISON. 1992. MacClade. Vers. 3. Sinauer, Sunderland, MA.
60. MAIER, W. 1987a. The ontogenetic development of the orbitotemporal region in the skull of Monodelphis domestica (Didelphidae, Marsupialia), and the problem of the mammalian alisphenoid. Pp. 71-90 in J.-J. Zeller and U. Kuhn, eds. Morphogenesis of the mammalian skull. Paul Pary, Hamburg.
61. _. 1987b. Der Processes angularis bei Monodelphis domestica (Didelphidae: Marsupialia) und seine Beziehungen zum Mittelohr: eine ontogenetische und evolutionsmorphologische Untersuchung. Gegen. Morph. Jahr. 133:123-161.
62. _. 1993. Cranial morphology of the therian common ancestor, as suggested by the adaptations of neonatal marsupials. Pp. 165-181 in F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds. Mammal phylogeny - Mesozoic differentiation, multituberculates, monotremes, early therians and marsupials. Springer, New York.
63. MARSHALL, L. G., J. A. CASE, AND M. O. WOODBURNE. 1990. Phylogenetic relationships of the families of marsupials. Pp. 433-502 in . H. H. Genoways, ed. Current mammalogy. Vol. 2. Plenum, New York.
64. MCCRADY, E. 1938. The embryology of the opossum. Memoirs of the Wistar Institution, Philadelphia, PA.
65. MCKINNEY, M. L. 1988. Heterochrony in evolution. Plenum, New York.
66. MIYAKE, T., A. M. CAMERON, AND B. K. HALL. 1996. Stage-specific onset of condensation and matrix deposition for Meckel's and other first arch cartilages in inbred C57B1/6 mice. J. Craniof. Genet. Devel. Biol. 16:32-47.
67. MOSS, M. L. 1968. A theoretical analysis of the functional matrix. Acta Biotheo. 18:195-202.
68. MOSS, M. L., AND L. SALENTIJIN. 1969. The primary role of functional matrices in facial growth. Am. J. Orthodon.s 55:566-577.
69. MÜLLER, F. 1972a. Zur stammesgeschichtlichen Veranderung der Eutheria-Ontogenesen. Versuch einer ubersieht aufgrund vergleichend morphologischer Studien an Marsupialia und Eutheria. I. Rev. Suisse Zool. 79:1-97.
70. _. 1972b. Zur stammesgeschichtlichen Veranderung der Eutheria-Ontogenesen. Versuch einer ubersieht aufgrund vergleichend morphologischer Studien an Marsupialia und Eutheria. II. Rev. Suisse Zool. 79:501-566.
71. _. 1972c. Zur stammesgeschichtlichen Veranderung der Eutheria-Ontogenesen. Versuch einer Ubersicht aufgrund vergleichend morphologischer Studien an Marsupialia und Eutheria. III. Rev. Suisse Zool. 79:567-611.
72. _. 1973. Zur Stammesgeschichtlichen Veranderung der Eutheria-Ontogenesen. Versuch einer Ubersicht aufgrund vergleichend morphologischer Studien an Marsupialia und Eutheria. IV. Rev. Suisse Zool. 79:1599-1685.
73. NELSON, J. E. 1987. The early development of the eye of the pouch-young of the marsupial Dasyurus hallucatus. Anat. Embry. 175: 387-398.
74. _. 1988. Growth of the Brain. Pp. 86-100 in C. H. Tyndale-Biscoe and P. A. Janssens, eds. The developing marsupial. Springer, Berlin.
75. _. 1992. Developmental staging in a marsupial Dasyurus hallucatus. Anat. Embry. 185:335-354.
76. NESSLINGER, C. L. 1956. Ossification centers and skeletal development in the postnatal Virginia opossum. J. Mamm. 37:382-394.
77. NODEN, D. M., AND A. DE LAHUNTA. 1985. The embryology of domestic animals. Williams and Wilkins, Baltimore, MD.
78. NOVACEK, M. J. 1990. Morphology, paleontology and the higher clades of mammals. Pp. 507-543 in H. H. Genoways, ed. Current mammalogy. Vol. 2. Plenum, New York.
79. NOVACEK, M. J., AND A. R. WYSS. 1986. Higher-level relationships of the recent eutherian orders: morphological evidence. Cladistics 2:257-287.
80. NOWAK, R. M., 1991. Walker's mammals of the world. 5th ed. Vol. 1. Johns Hopkins Univ. Press, Baltimore, MD.
81. PARKER, P. 1977. An ecological comparison of marsupial and pla cental patterns of reproduction. Pp. 273-286 in B. Stonehouse and D. Gilmore, eds. The biology of marsupials. Macmillan, London.
82. RENFREE, M. B. 1983. Marsupial reproduction: The choice between placentation and lactation. Pp. 1-29 in C. A. Finn, ed. Oxford reviews of reproductive biology. Vol. 5. Oxford Univ. Press, Oxford.
83. _. 1993. Ontogeny, genetic control, and phylogeny of female reproduction in monotreme and therian mammals. Pp. 4-20 in F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds. Mammal phylogeny - Mesozoic, differentiation, multituberculates, monotremes, early therians and marsupials. Springer, New York.
84. RENFREE, M. B., A. B. HOLT, S. W. GREEN, J. P. CARR, AND D. B. CHEEK. 1982. Ontogeny of the brain in a marsupial (Macropus eugenii) throughout pouch life. Brain, Beha. Evol. 20:57-71.
85. REYNOLDS, M. L., AND N. R. SAUNDERS. 1988. Differentiation of the neocortex. Pp. 101-116 in C. H. Tyndale-Biscoe and P. A. Janssens, eds. The developing marsupial. Springer, Berlin.
86. RUSSELL, E. 1982a. Patterns of parental care and parental investment in marsupials. Biol. Rev. 57:423-486.
87. _. 1982b. Parental investment and desertion of young in marsupials. Am. Nat. 119:744-748.
88. SACHER, G. A., AND E. F. STAFFELDT. 1974. Relation of gestation time to brain weight for placental mammals: implications for the theory of vertebrate growth. Am. Nat. 108:593-615.
89. SAUNDERS, N. R., E. ADAM, M. READER, AND K. MOLLGARD. 1989. Monodelphis domestica (gray short-tailed opossum): an accessible model for studies of early neocortical development. Anat. Embry. 180:227-236.
90. SCHOWING, J. 1961. Influence inductrice de l'encéphale et de la chorde sur la morphogenèse du squellette cranien chez l'embryon de Poulet. J. Embry. Exp. Morph. 9:326-334.
91. _. 1968. Mise en évidence du rôle inducteur de l'encéphale dans l'ostéogenèse du crâne embryonnaire du poulet. J. Embry. Exp. Morph. 19:88-93.
92. SHARMAN, G. B. 1973. Adaptations of marsupial pouch young for extrauterine existence. Pp. 67-90 in C. R. Austin, ed. The mammalian fetus in vitro. Chapman and Hall, London.
93. SHOEMAKER, W. J., AND F. E. BLOOM. 1977. Effect of undernutrition on brain morphology. Pp. 147-192 in. R. J. Wurtman and J. J. Wurtman eds. Nutrition and the brain. Vol. 2. Raven Press, New York.
94. SMITH, K. K. 1994. The development of craniofacial musculature in Monodelphis domestica (Didelphidae, Marsupialia). J. Morph. 222:149-173.
95. _. 1996. Integration of craniofacial structures during development in mammals. Am. Zool. 36:70-79.
96. STRAUSS, R. E. 1990. Heterochronic variation in the developmental timing of cranial ossification in poeciliid fishes (Cryprinodontiformes). Evolution 44:1558-1567.
97. SZALAY, F. S. 1994. Evolutionary history of the marsupials and an analysis of osteological characters. Cambridge Univ. Press, Cambridge.
98. THEILER, K. 1989. The house mouse. Developmental and normal stages from fertilization to 4 weeks of age. Springer, Berlin.
99. THOMPSON, S. D. 1987. Body size, duration of parental care, and the intrinsic rate of natural increase in eutherian and metatherian mammals. Oecologia 71:201-209.
100. THOMPSON, S. D., AND M. E. NICOLL. 1986. Basal metabolic rate and energetics of reproduction in therian mammals. Nature, Lond. 321:690-693.
101. THOROGOOD, P. 1988. The developmental specification of the vertebrate skull. Development (supplement) 103:141-153.
102. THOROGOOD, P., J. BEE, AND K. VON DER MARK. 1986. Transient expression of collagen type II at epitheliomesenchymal interfaces during morphogenesis of the cartilaginous neurocranium. Devel. Biol. 116:497-509.
103. TYLER, M. S. 1978. Epithelial influences on membrane bone formation in the maxilla of the embryonic chick. Anat. Rec. 192: 225-234.
104. _. 1983. Development of the frontal bone and cranial meninges in the embryonic chick: an experimental study of tissue interactions. Anat. Rec. 206:61-70
105. _. 1988. Development of osteogenic and chondrogenic potentials along the mediolateral axis of the embryonic chick mandible. Arch. Oral Biol. 33:443-449.
106. TYNDALE-BISCOE, C. H. 1973. Life of marsupials. Edward Arnold, London.
107. TYNDALE-BISCOE, C. H., AND M. RENFREE. 1987. Reproductive physiology of marsupials. Cambridge Univ. Press, Cambridge.
108. VELHAGEN, W. A. 1995. A comparative study of cranial development in the thamnophiine snakes (Serpentes: Colubridae). Ph.D. diss. Duke Univ. Durham, NC.
109. WAKE, M. H., AND J. HANKEN. 1982. The development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J. Morph. 173:203-223.
110. WINICK, M. 1976. Malnutrition and brain development. Oxford Univ. Press, New York.
111. _. 1979. Nutrition, pre- and postnatal development. Plenum, New York
112. WINICK, M., P. ROSSO, AND J. A. BRASEL. 1972. Malnutrition and cellular growth in the brain: existence of critical periods. Pp. 200-206 in Lipids, malnutrition and the developing brain, Ciba Foundation symposium. Elsevier/North Holland, Amsterdam.
113. WOOD, A., D. E. ASHHURST, A. CORBETT, AND P. THOROGOOD. 1991. The transient expression of type II collagen at tissue interfaces during mammalian craniofacial development. Development 111: 955-968.