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Craniofacial development in marsupial mammals: Developmental origins of evolutionary change

  1. Kathleen K. Smith*

Article first published online: 11 JAN 2006

DOI: 10.1002/dvdy.20676

Issue

Developmental Dynamics

Developmental Dynamics

Special Issue: Craniofacial Development Special Issue

Volume 235, Issue 5, pages 1181–1193, May 2006

Additional Information

How to Cite

Smith, K. K. (2006), Craniofacial development in marsupial mammals: Developmental origins of evolutionary change. Dev. Dyn., 235: 1181–1193. doi: 10.1002/dvdy.20676

Author Information

  1. Department of Biology, Duke University, Durham, North Carolina

*Box 90338, Duke University, Durham NC 27708

Publication History

  1. Issue published online: 19 APR 2006
  2. Article first published online: 11 JAN 2006
  3. Manuscript Accepted: 28 NOV 2005

Funded by

  • NSF. Grant Number: IBN 0316353

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REFERENCES

  • Aiello LE, Wheeler P. 1995. The expensive-tissue hypothesis. Curr Anthro 36: 199–221.
  • Alberch P. 1980. Ontogenesis and morphological diversification. Am Zool 20: 653–667.
  • Ciffelli RL, Rowe TB, Luckett WP, Banta J, Reyes R, Howes RI. 1996. Fossil evidence for the origin of the marsupial pattern of tooth replacement. Nature 379: 715–719.
  • Clark CT, Smith KK. 1993. Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J Morphol 215: 119–149.
    Direct Link:
  • Cockburn A. 1989. Adaptive patterns in marsupial reproduction. Trends Ecol Evo 4: 126–130.
  • Couly GF, Coltey PM, Le Douarin NM. 1993. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117: 409–429.
  • Couly GF, Grapin-Botton A, Coltey P, Ruhin B, Le Douarin NM. 1998. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125: 3445–3459.
  • Cruz YP, Yousef A, Selwood L. 1996. Fate-map analysis of the epiblast of the Dasyurid marsupial Sminthopsis macroura. Reprod Fertil Dev 8: 779–788.
  • Eisenberg JF. 1981. The Mammalian Radiations. Chicago: University of Chicago Press. 610 p.
  • Epperlein HH, Löfberg J. 1993. The development of the neural crest in amphibians. Ann Anat 175: 483–499.
  • Fadem BH, Trupin GL, Maliniak E, VandeBerg JL, Hayssen V. 1982. Care and breeding of the gray, short-tailed opossum (Monodelphis domestica). Lab Anim Sci 32: 405–409.
  • Falck P, Joss J, Olsson L. 2000. Cranial neural crest cell migration in the Australian lungfish, Neoceratodus forsteri. Evol Dev 2: 179–185.
    Direct Link:
  • Filan SL. 1991. Development of the middle ear region in Monodelphis domestica (Marsupialia, Didelphidae): marsupial solutions to early birth. J Zool Lond 225: 577–588.
    Direct Link:
  • Fish JL, Lockwood CA. 2003. Dietary constraints on encephalization in primates. Am J Phys Anthro 120: 171–181.
    Direct Link:
  • Frigo L, Woolley PA. 1996. Development of the skeleton of the stripe-faced dunnart, Sminthopsis macroura (Marsupialia: Dasyuridae). Aust J Zool 44: 155–164.
  • Gavalas A, Studer M, Lumsden A, Rijli FM, Krumlauf R, Chambon P. 1998. Hoxa1 and Hoxb1 synergize in patterning the hindbrain, cranial nerves and second pharyngeal arch. Development 125: 1123–1136.
  • Gemmell RT, Nelson J. 1988a. The ultrastructure of the lung of two newborn marsupial species, the northern native cat, Dasyurus hallucatus, and the brushtail possum, Trichosurus vulpecula. Cell Tissue Res 252: 683–685.
  • Gemmell RT, Nelson J. 1988b. Ultrastructure of the olfactory system of three newborn marsupial species. Anat Rec 221: 655–662.
    Direct Link:
  • Gemmell RT, Nelson J. 1992. Development of the vestibular and auditory system of the northern native cat, Dasyurus hallucatus. Anat Rec 234: 136–143.
    Direct Link:
  • Gemmell RT, Selwood L. 1994. Structural development in the newborn marsupial, the stripe-faced dunnart, Sminthopsis macroura. Acta Anat 149: 1–12.
  • Hall BK. 1999. The neural crest in development and evolution. New York: Springer-Verlag. 313 p.
  • Hall BK, Horstadius S. 1988. The neural crest. London: Oxford University Press. 303 p.
  • Hall LS, Hughes RL. 1987. An evolutionary perspective of structural adaptations for environmental perception and utilization by the neonatal marsupials Trichosurus vulpecula (Phalangeridae) and Didelphis virginiana (Didelphidae). In: ArcherM, editor. Possums and opossums: studies in evolution. Sydney: Surrey Beatty and Sons. p 257–251.
  • 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 Morphol 177: 255–268.
    Direct Link:
  • Hanken J. Jennings DH, Olsson L. 1997. Mechanistic basis of life-history evolution in anuran amphibians: direct development. Am Zool 37: 160–171.
  • Hayssen V, Lacy RC, Parker PJ. 1985. Metatherian reproduction: transitional or transcending? Am Nat 126: 617–632.
  • Herring SW. 1993. Epigenetic and functional influences on skull growth. In: HankenJ, HallBK, editors. The skull. Vol. 1. Chicago: University of Chicago Press. p 153–206.
  • Hidalgo-Sanchez M, Alvarado-Mallart RM. 2002. Temporal sequence of gene expression leading caudal prosencephalon to develop a midbrain/hindbrain phenotype. Dev Dyn 223: 141–147.
    Direct Link:
  • Hill JP, Watson KM. 1958. The early development of the brain in marsupials. Preliminary communication. J Anat 92: 493–497.
  • Hill JP, Hill WCO. 1955. The growth stages of the pouch young of the native cat (Dasyurus viverrinus) together with observations on the anatomy of the new born young. Trans Zool Soc Lond 28: 349–453.
    Direct Link:
  • Horigome N, Myojin M, Uek T, Hirano S, Aizawa SKS. 1999. Development of cephalic neural crest cells in embryos of Lampetra japonica, with special reference to the evolution of the jaw. Dev Bio 207: 287–308.
  • Hughes RL, Hall LS. 1988. Structural adaptations of the newborn marsupial. In: Tyndale-BiscoeCH, JanssensPA, editors. The developing marsupial. Berlin: Springer-Verlag. p 8–27.
  • Irving C, Mason I. 1999. Regeneration of isthmic tissue is the result of a specific and direct interaction between rhombomere 1 and midbrain. Development 126: 3981–3989.
  • Irving C, Mason I. 2000. Signaling by FGF8 from the isthmus patterns anterior hindbrain and establishes the anterior limit of Hox gene expression. Development 127: 177–186.
  • Jernvall J. 1995. Mammalian molar cusp patterns: developmental mechanisms of diversity. Acta Zool Fenn 198: 1–61.
  • Joyner AL, Liu A, Millet S. 2000. Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr Opin Cell Biol 12: 736–741.
  • Kaufman MH, Bard JBL. 1999. The anatomical basis of mouse development. New York: Academic Press. 291 p.
  • Kay E. 1986. The phenotypic interdependence of the musculoskeletal characters of the mandibular arch in mice. J Embryol Exp Morphol 98: 123–136.
  • Keynes R, Lumsden A. 1990. Segmentation and the origin of regional diversity in the vertebrate central nervous system. Neuron 2: 1–9.
  • Kirkpatrick TH. 1978. The development of the dentition of Macropus giganteus (Shaw): an attempt to interpret the marsupial dentition. Aust Mammal 2: 29–35.
  • Kirsch JAW. 1977a. Biological aspects of the marsupial-placental dichotomy: a reply to Lillegraven. Evolution 31: 898–900.
  • Kirsch JAW. 1977b. The six-percent solution: second thoughts on the adaptedness of the Marsupialia. Am Sci 65: 276–288.
  • Klima M. 1987. Early development of the shoulder girdle and sternum in marsupials (Mammalia: Metatheria). Adv Anat Embryol Cell Biol 109: 1–91.
  • Klima M, Bangma GC. 1987. Unpublished drawings of marsupial embryos from the Hill collection and some problems of marsupial ontogeny. Zeit Saugetier 52: 201–211.
  • Köntges G, Lumsden A. 1996. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122: 3229–3242.
  • Krause WJ. 1998. A review of histogenesis/organogenesis in the developing North American opossum. Adv Anat Embryol Cell Biol 143: 1–120.
  • Krause WJ, Saunders NR. 1994. Brain growth and neocortical development in the opossum. Ann Anat 176: 395–407.
  • Larsen WJ. 2001. Human embryology. New York: Churchill Livingstone. 548 p.
  • Le Douarin NM, Kalcheim C. 1999. The neural crest. Cambridge: Cambridge University Press. 469 p.
  • Lee AK, Cockburn A. 1985. Evolutionary ecology of marsupials. Cambridge: Cambridge University Press. 274 p.
  • Lee SM, Danielian PS, Fritzsch B, McMahon AP. 1997. Evidence that FGF8 signaling from the midbrain-hindbrain junction regulates growth and polarity in the developing midbrain. Development 124: 959–969.
  • Leigh SR. 2004. Brain growth, life history, and cognition in primate and human evolution. Am J Primat 62: 139–164.
    Direct Link:
  • Lillegraven JA. 1975. Biological considerations of the marsupial-placental dichotomy. Evolution 29: 707–722.
  • Lillegraven JA, Thompson SD, McNab BK, Patton JL. 1987. The origin of eutherian mammals. Biol J Linn Soc 32: 281–336.
    Direct Link:
  • Luckett WP. 1993. An ontogenetic assessment of dental homologies in therian mammals. In: SzalayFS, NovacekMJ, McKennaMC., editors. Mammal phylogeny. Vol. 1. New York: Springer. p 182–204.
  • Luckett WP, Woolley PA. 1996. Ontogeny and homology of the dentition in dasyurid marsupials: development in Sminthopsis virginiae. J Mamm Evol 3: 327–364.
  • Lumsden A, Krumlauf R. 1996. Patterning the vertebrate neuraxis. Science 274: 1109–1115.
  • Maier W. 1993. Cranial morphology of the therian common ancestor, as suggested by the adaptations of neonatal marsupials. In: SzalayFS, NovacekMJ, McKennaMC, editors. Mammal phylogeny. Vol. 1. New York: Springer. p 165–181.
  • Maier W. 1999. On the evolutionary biology of early mammals — with methodological remarks on the interaction between ontogenetic adaptation and phylogenetic transformation. Zool Anz 238: 55–74.
  • Martinez S. 2001. The isthmic organizer and brain regionalization. Int J Dev Biol 44: 367–371.
  • Mason I, Chambers D, Shamin H, Walshe J, Irving C. 2000. Regulation and function of FGF8 in patterning of midbrain and anterior hindbrain. Biochem Cell Biol 78: 577–584.
  • Mate KE, Robinson ES, VandeBerg JL, Pedersen RA. 1994. Timetable of in vivo embryonic development in the grey short-tailed opossum (Monodelphis domestica). Mol Reprod Dev 39: 365–374.
    Direct Link:
  • McCrady E. 1938. The embryology of the opossum. Philadelphia: Wistar Institute of Anatomy and Biology. 233 p.
  • Morriss-Kay G, Ruberte E, Fukiishi Y. 1993. Mammalian neural crest and neural crest derivatives. Ann Anat 175: 501–507.
  • Moss ML, Salentijin L. 1969. The primary role of functional matrices in facial growth. Am J Orthodont 55: 566–577.
  • Nelson JE. 1987. The early development of the eye of the pouch-young of the marsupial Dasyurus hallucatus. Anat Embryol (Berl) 175: 387–398.
  • Nelson JE. 1988. Growth of the brain. In: Tyndale-BiscoeCH, JanssensPA, editors. The developing marsupial. Berlin: Springer Verlag. p 86–100.
  • Nesslinger CL. 1956. Ossification centers and skeletal development in the postnatal Virginia opossum. J Mamm 37: 382–394.
  • Nichols DH. 1981. Neural crest formation in the head of the mouse embryo as observed using a new histological technique. J Embryol Exp Morphol 64: 105–120.
  • Nichols DH. 1987. Ultrastructure of neural crest formation in the midbrain/rostral hindbrain and periotic hindbrain regions of the mouse embryo. Am J Anat 179: 143–154.
    Direct Link:
  • Nijhout HF, Emlen DJ. 1998. Competition among body parts in the development and evolution of insect morphology. Proc Natl Acad Sci U S A 95: 3685–3689.
  • Noden DM. 1983. The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96: 144–165.
  • Noden DM. 1984. Craniofacial development: new views on old problems. Anat Rec 208: 1–13.
    Direct Link:
  • Noden DM. 1988. Interactions and fates of avian craniofacial mesenchyme. Development 103: 121–140.
  • Noden DM, De Lahunta A. 1985. The embryology of domestic animals. Baltimore: Williams and Wilkins. 367 p.
  • Nowicki S, Searcy WA. 2004. Song functions and the evolution of female preferences. Ann N Y Acad Sci 1016: 704–723.
    Direct Link:
  • Nowicki S, Searcy WA, Peters S. 2002. Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Phys 188: 1003–1014.
  • Nunn CL, Smith KK. 1998. Statistical analysis of developmental sequences: the craniofacial region in marsupial and placental mammals. Am Nat 152: 82–101.
  • Osumi-Yamashita N, Ninomiya Y, Doi H, Eto K. 1994. The contribution of both forebrain and midbrain crest cells to the mesenchyme in the frontonasal mass of mouse embryos. Development 164: 409–419.
  • Osumi-Yamashita N, Ninomiya Y, Doi H, Eto K. 1996. Rhombomere formation and hind-brain crest cell migration from prorhombomeric origins in mouse embryos. Dev Growth Differ 38: 107–118.
    Direct Link:
  • Parker P. 1977. An ecological comparison of marsupial and placental patterns of reproduction. In: StonehouseB, GilmoreD, editors. The biology of marsupials. London: Macmillan Press Ltd. p 273–286.
  • Piotrowski T, Nusslein-Volhard C. 2000. The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish (Danio rerio). Dev Biol 225: 339–356.
  • Prince V, Lumsden A. 1994. Hoxa-2 expression in normal and transposed rhombomeres: independent regulation in the neural tube and neural crest. Development 120: 911–923.
  • Raff RA. 1996. The shape of life. Chicago: University of Chicago Press. 520 p.
  • Renfree MB. 1983. Marsupial reproduction: the choice between placentation and lactation. In: FinnA, editor. Oxford reviews of reproductive biology. Oxford: Oxford University Press. p 1–29.
  • Renfree MB. 1995. Monotreme and marsupial reproduction. Reprod Fertil Dev 7: 1003–1020.
  • Ruberte E, Wood HB, Morriss-Kay GM. 1997. Prorhombomeric subdivision of the mammalian embryonic hindbrain: is it functionally meaningful? Int J Dev Biol 41: 213–222.
  • Saunders NR, Adam E, Reader M, Mollgard K. 1989. Monodelphis domestica (grey short-tailed opossum): an accessible model for studies of early neocortical development. Anat Embryol (Berl) 180: 227–236.
  • Schneider RA, Helms JA. 2003. The cellular and molecular origins of beak morphology. Science 299: 565–568.
  • Schowing J. 1968. Mise in evidence du role inducteur de l'encephale dans l'osteogenese du crane embryonnaire du poulet. J Embryol Exp Morphol 19: 88–93.
  • Sears KE. 2004. Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58: 2353–2370.
  • Selwood L, Robinson ES, Pedersen RA, VandeBerg JL. 1997. Development in vitro of marsupials: a comparative review of species and a timetable of cleavage and early blastocyst stages of development in Monodelphis domestica. Int J Dev Biol 41: 397–410.
  • Selwood L, VandeBerg JL. 1992. The influence of incubation temperature on oocyte maturation, parthenogenetic and embryonic development in vitro of the marsupial Monodelphis domestica. Anim Reprod Sci 29: 99–116.
  • Serbedzija GN, Bronner-Fraser M, Fraser SE. 1992. Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116: 297–307.
  • Shamin H, Mahmood R, Logan C, Doherty P, Lumsden A, Mason I. 1999. Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 126: 945–959.
  • Smith KK. 1992. The evolution of the mammalian pharynx. Zool J Linnaean Soc 104: 313–349.
    Direct Link:
  • Smith KK. 1994. The development of craniofacial musculature in Monodelphis domestica (Didelphidae, Marsupialia). J Morphol 222: 149–173.
    Direct Link:
  • Smith KK. 1996. Integration of craniofacial structures during development in mammals. Am Zool 36: 70–79.
  • Smith KK. 1997. Comparative patterns of craniofacial development in eutherian and metatherian mammals. Evolution 51: 1663–1678.
  • Smith KK. 2001a. Early development of the neural plate, neural crest and facial region of marsupials. J Anat 199: 121–131.
  • Smith KK. 2001b. The evolution of mammalian development. Bull Mus Comp Zool 156: 119–135.
  • Smith KK. 2001c. Heterochrony revisited: the evolution of developmental sequences. Biol J Linn Soc 73: 169–186.
    Direct Link:
  • Smith KK. 2002. Sequence heterochrony and the evolution of development. J Morphol 252: 82–97.
    Direct Link:
  • Smith KK. 2003. Time's arrow: heterochrony and the evolution of development. Int J Dev Biol 47: 613–621.
  • Tan SS, Morriss-Kay GM. 1985. The development and distribution of the cranial neural crest in the rat embryo. Cell Tissue Res 240: 403–416.
  • Tan SS, Morriss-Kay GM. 1986. Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimeras. J Embryol Exp Morphol 98: 21–58.
  • Tosney KW. 1982. The segregation and early migration of cranial neural crest cells in the avian embryo. Dev Biol 89: 13–24.
  • Trainor PA, Krumlauf R. 2000. Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat Cell Biol 2: 96–102.
  • Trainor PA, Krumlauf R. 2001. Hox genes, neural crest cells and branchial arch patterning. Curr Opin Cell Biol 13: 698–705.
  • Trainor PA, Ariza-McNaughton L, Krumlauf R. 2002. Role of the isthmus and FGFs in resolving the paradox of neural crest plasticity and prepatterning. Science 295: 1288–1291.
  • Tyndale-Biscoe H. 1973. Life of marsupials. London: Edward Arnold (Publ.) Ltd.
  • Tyndale-Biscoe H, Renfree M. 1987. Reproductive physiology of marsupials. Cambridge: Cambridge University Press. 476 p.
  • Vaglia J, Smith KK. 2003. Early differentiation and migration of cranial neural crest in the opossum, Monodelphis domestica. Evol Dev 5: 121–135.
    Direct Link:
  • van Nievelt AFH, Smith KK. 2005a. To replace or not to replace: the significance of reduced functional tooth replacement in marsupial and placental mammals. Paleobiology 31: 324–346.
  • van Nievelt AFH, Smith KK. 2005b. Tooth eruption in Monodelphis domestica and its significance for phylogeny and natural history. J Mamm 86: 333–341.
  • VandeBerg JL. 1983. The grey short-tailed opossum: a new laboratory animal. Inst Lab Anim Res News 26: 9–12.
  • Veitch E, Begbie J, Schilling T, Smith MM, Graham A. 1999. Pharyngeal arch patterning in the absence of neural crest. Curr Biol 9: 1481–1484.
  • Wilson JT, Hill JP. 1897. Observations upon the development and succession of the teeth in Perameles; together with a contribution to the discussion of the homologies of the teeth in marsupial animals. Q J Micros Sci 39: 427–588.
  • Winge H. 1941. The interrelationships of the mammalian genera. Vol. 1. Copenhagen: CA Reitzel.
  • Ziegler AC. 1971. A theory of the evolution of therian dental formulas and replacement patterns. Q Rev Biol 46: 226–249.
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