Journal of Mammalian Evolution

, Volume 12, Issue 3–4, pp 303–336 | Cite as

Organization of the Olfactory and Respiratory Skeleton in the Nose of the Gray Short-Tailed Opossum Monodelphis domestica

  • Timothy B. Rowe
  • Thomas P. Eiting
  • Thomas E. Macrini
  • Richard A. Ketcham
Comparative Morphology and Early Diversification of Mammals

Abstract

The internal nasal skeleton in Monodelphisdomestica, the gray short-tailed opossum, primarily supports olfactory and respiratory epithelia, the vomeronasal organ, and the nasal gland. This scaffold is built by the median mesethmoid, and the paired vomer and ethmoid bones. The mesethmoid ossifies within the nasal septum cartilage. The bilateral ethmoid segregates respiratory and olfactory regions, and its geometry offers insight into the functional, developmental, and genomic organization of the nose. It forms through partial coalescence of separate elements known as turbinals, which in Monodelphis comprise the maxilloturbinal, nasoturbinal, five endoturbinals, and two ectoturbinals. Geometry of the ethmoid increases respiratory mucosal surface area by a factor of six and olfactory mucosal surface by nearly an order of magnitude. Respiratory epithelium warms and humidifies inspired air, recovers moisture as air is exhaled, and may help mediate brain temperature. In contrast, the olfactory skeleton functions as a series of small funnels that support growth of new olfactory neurons throughout life. Olfactory mucosa lines the mouth of each funnel, forming blind olfactory recesses known as the ethmoid cells, and neuronal axons are funneled from the epithelium through tiny olfactory foramina in the cribriform plate, into close proximity with target glomeruli in the olfactory bulb of the brain where each axon makes its first synapse. The skeleton may thus mediate topological correspondence between odorant receptor areas in the nose with particular glomeruli in the olfactory bulb, enabling growth throughout life of new olfactory neurons and proper targeting by their axons. The geometric arrangement of odorant receptors suggests that a measure of volatility may be a component in the peripheral olfactory code, and that corresponding glomeruli may function in temporal signal processing. Supporting visualizations for this study are available online at www.DigiMorph.org.

Key Words

Vomeronasal organ Mesethmoid Ethmoid Turbinals Vomer Computed tomography 

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References

  1. Allen, H. (1882). On a revision of the ethmoid bone in the Mammalia. Bull. Mus. Comp. Zool. 10: 135–164.Google Scholar
  2. Berlingrood, M. (1969). A Study of the Outgrowth and Pathway Determination of Nerve Fibers in the Newt, Ph.D. Dissertation, The University of Texas at Austin.Google Scholar
  3. Bloom, W., and Fawcett, D. W. (1975). A Textbook of Histology, 10th Ed., W. B. Saunders Company, Philadelphia.Google Scholar
  4. Brown, J. W. (1987). The nervus terminalis in insectivorous bat embryos and notes on its presence during human ontogeny. Ann. N. Y. Acad. Sci. 519: 174–183.Google Scholar
  5. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: A molecular basis of odor recognition. Cell 65: 175–187.PubMedCrossRefGoogle Scholar
  6. Butler, A. B., and Hodos, W. (1996). Comparative Vertebrate Neuroanatomy, Wiley, New York.Google Scholar
  7. Carlson, W. D., Rowe, T., Ketcham, R. A., and Colbert, M. W. (2003). Geological applications of high-resolution X-ray computed tomography in petrology, meteoritics and palaeontology. In: Applications of X-ray Computed Tomography in the Geosciences, Vol. 215, F. Mees, R. Swennen, M. Van Geet, and P. Jacobs, eds., pp. 7–22, Geological Society, London.Google Scholar
  8. Clark, C. T., and Smith, K. K. (1993). Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J. Morphol. 215: 119–149.PubMedCrossRefGoogle Scholar
  9. Cleland, J. (1862). On the relations of the vomer, ethmoid, and intermaxillary bones. Phil. Trans. R. Soc. Lond. 152: 289–321.Google Scholar
  10. Colbert, M. W., Racicot, R., and Rowe, T. (2005). Anatomy of the cranial endocast of the bottlenose dolphin Tursiops truncatus, based on HRXCT. J. Mamm. Evol. 12 (in press).Google Scholar
  11. Coues, E. (1872). On the osteology and myology of Didelphis virginiana. Mem. Boston Soc. Nat. Hist. 2: 41–154.Google Scholar
  12. De Beer, G. R. (1937). The Development of the Vertebrate Skull, Oxford University Press, Oxford.Google Scholar
  13. Del Punta, K., Leinders-Zufall, T., Rodriguez, I., Jukam, D., Wysocki, C. J., Ogawa, S., Zufall, F., and Mombaerts, P. (2002). Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419: 70–74.PubMedCrossRefGoogle Scholar
  14. Demski, L. S. (1987). Phylogeny of lutenizing hormone-releasing hormone systems in protochordates and vertebrates. Ann. N. Y. Acad. Sci. 519: 1–14.PubMedGoogle Scholar
  15. Ducham-Viret, P., Chaput, M. A., and Duchamp, A. (1999). Odor response properties of rat olfactory receptor neurons. Science 284: 2171–2174.Google Scholar
  16. Dreyer, W. (1998). The area code hypotheses revisited: Olfactory receptors and other related transmembrane receptors may function as the last digits in a cell surface code for assembling embryos. Proc. Natl. Acad. Sci. U.S.A. 95: 9072–9077.PubMedCrossRefGoogle Scholar
  17. Dryer, L. (2000). Evolution of odorant receptors. BioEssays 22: 803–810.PubMedCrossRefGoogle Scholar
  18. Firestein, S. (2001). How the olfactory system makes sense of scents. Nature 413: 211–218.PubMedCrossRefGoogle Scholar
  19. Gauthier, J., Kluge, A. G., and Rowe, T. (1988). Amniote phylogeny and the importance of fossils. Cladistics 4: 105–209.CrossRefGoogle Scholar
  20. Gheusi, G., Cremer, H., McLean, H., Chazal, G., Vincent, J-D., and Lledo, P.-M. (2000). Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc. Natl. Acad. Sci. U.S.A. 97: 1823–1828.PubMedCrossRefGoogle Scholar
  21. Godfrey, P. A., Malnic, B., and Buck, L. B. (2004). The mouse olfactory receptor gene family. Proc. Natl. Acad. Sci. U.S.A. 101: 2156–2161.PubMedCrossRefGoogle Scholar
  22. Goldberg, M. B., Langman, V. A., and Taylor, C. R. (1981). Panting in dogs: Paths of air flow in response to heat and exercise. Respir. Physiol. 43: 327–338.PubMedCrossRefGoogle Scholar
  23. Gregory, W. K. (1910). The orders of mammals. Bull. Am. Mus. Nat. Hist. 27: 1–524.Google Scholar
  24. Hall, B. K. (1990). Tissue interactions in the development and evolution of the vertebrate head. In: Developmental and Evolutionary Aspects of the Neural Crest, P. F. A. Maderson, ed., pp. 159–260, Wiley, New York.Google Scholar
  25. Harrison, R. J. (1972). Functional Anatomy of Marine Mammals, Academic Press, London.Google Scholar
  26. Hillenius, W. J. (1992). The evolution of nasal turbinates and mammalian endothermy. Paleobiology 18: 17–29.Google Scholar
  27. Kay, R. F., Campbell, V. M., Rossis, J. B., Colbert, M. W., and Rowe, T. B. (2004). The olfactory system of Tremacebus harringtoni (Platyrhini, early Miocene, Cacanana, Argentina): Implications for activity pattern. Anat. Rec. (A) 281A: 1157–1172.Google Scholar
  28. Ketcham, R. A., and Carlson, W. D. (2001). Acquisition, optimization and interpretation of X-ray computed tomographic imagery: Applications to the geosciences. Comput. Geosci. 27: 381–400.Google Scholar
  29. Ketcham, R. A. (2005). Computer methods for quantitative analysis of three-dimensional features in geological specimens. Geosphere 1: 32–41.Google Scholar
  30. Keverne, E. B. (1999). The vomeronasal organ. Science 286: 716–720.PubMedCrossRefGoogle Scholar
  31. Lane, R. P., Cutforth, T., Young, J., Athanasiou, M., Friedman, C., Rowen, L., Evans, G., Axel, R., Hood, L., and Trask, B. J. (2001). Genomic analysis of orthologous mouse and human olfactory receptor loci. Proc. Natl. Acad. Sci. U.S.A. 98: 7390–7395.PubMedCrossRefGoogle Scholar
  32. Laurent, G. (1999). A systems perspective on early olfactory coding. Science 286: 723–728.PubMedCrossRefGoogle Scholar
  33. Ma, M., and Sheppard, G. M. (2000). Functional mosaic organization of mouse olfactory receptor neurons. Proc. Natl. Acad. Sci. U.S.A. 97: 12869–12874.PubMedGoogle Scholar
  34. Macrini, T. E. (2000). High Resolution X-ray Computed Tomography (CT) of the Skull of an Extant Opossum (Monodelphis domestica) and a Comparison of its Ontogeny to Synapsid Phylogeny, Unpublished M. S. Thesis, The University of Texas at Austin, Austin.Google Scholar
  35. Malnic, B., Godfrey, P. A., and Buck, L. B. (2004). The human olfactory receptor gene family. Proc. Natl. Acad. Sci. U.S.A. 101: 2584–2589.PubMedCrossRefGoogle Scholar
  36. Marshall, L. G., and de Muizon, C. (1995). Part II. The skull. In: Pucadelphys andinus (Marsupialia, Mammalia) from the early Paleocene of Bolivia, L. G. Marshall, C. de Muizon, and D. Signogneau-Russell, eds., Mém. Mus. Hist. Nat., Paris 165: 21–90.Google Scholar
  37. Mitchell, E., Maloney, S. K., Jessen, C., Laburn, H. P., Kamerman, P. R., Mitchell, G., and Fuller, A. (2002). Adaptive heterothermy and selective brain-cooling in arid-zone mammals. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131: 571–585.PubMedGoogle Scholar
  38. Mombaerts, P. (1999). Seven-transmembrane proteins as odorant and chemoreceptors. Science 286: 707–711.PubMedCrossRefGoogle Scholar
  39. Mombaerts, P., Wang, F., Dulac, C., Chao, S. K., Nemes, A., Mendelsohn, M., Edmondson, J., and Axel, R. (1996). Visualizing an Olfactory Sensory Map. Cell 87: 675–686.PubMedCrossRefGoogle Scholar
  40. Moore, W. J. (1981). The Mammalian Skull, Cambridge University Press, Cambridge, Massachusetts.Google Scholar
  41. Mori, K., Nagao, H., and Yoshihara, Y. (1999). The olfactory bulb: Coding and processing of odor molecule information. Science 286: 711–715.PubMedCrossRefGoogle Scholar
  42. Negus, V. (1958). The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses, Livingstone, Edinburgh.Google Scholar
  43. Nieuwenhuys, R., Ten Donkelaar, H. J., and Nicholson, C. (1998). The Central Nervous System of Vertebrates, Springer, Berlin.Google Scholar
  44. Niimura, Y., and Nei, M. (2003). Evolution of olfactory receptor genes in the human genome. Proc. Natl. Acad. Sci. U.S.A. 100: 12235–12240.PubMedCrossRefGoogle Scholar
  45. Noden, D. M. (1990). Interactions between cephalic neural crest and mesodermal populations. In: Developmental and Evolutionary Aspects of the Neural Crest, P. F. A. Maderson, ed., pp. 89–120, Wiley, New York.Google Scholar
  46. Novacek, M. J. (1993). Patterns of diversity on the mammalian skull. In: The Skull, Vol. 2, J. Hanken and B. K. Hall, eds., pp. 438–545, University of Chicago Press, Chicago.Google Scholar
  47. Owen, R. (1854). The Principal Forms of the Skeleton and of the Teeth, Blanchard and Lea, Philadelphia.Google Scholar
  48. Paulli, S. (1900a). Ueber die Pneumaticität des Schädels bei den Säugethieren. I. Ueber die Morphologie des Siebbeins und die Pneumaticität bei den Monotrematen und den Marsupialliern. Morph. Jb. 28: 147–178.Google Scholar
  49. Paulli, S. (1900b). Ueber die Pneumaticitat des Schadels bei den Saugethieren. II. Ueber die Morphologie des Siebbeins und die Pneumaticität bei den Ungulaten und Probosciden. Morph. Jb. 28: 179–251.Google Scholar
  50. Paulli, S. (1900c). Ueber die Pneumaticitat des Schadels bei den Saugethieren. III. Ueber die Morphologie des Siebbeins und die Pneumaticität bei den Insectivoren Hyracoideen, Chiropteren, Carnivoren, Pinnipeden, Edentates, Rodentiern, Prosimien und Primaten. Morph. Jb. 28: 483–564.Google Scholar
  51. Poran, N. S. (1998). Vomeronasal organ and its associated structures in the opossum Monodelphis domestica. Microsc. Res. Tech. 43: 500–510.PubMedCrossRefGoogle Scholar
  52. Proetz, A. W. (1953). Essays on the Applied Physiology of the Nose, 2nd Ed., Annals Publishing Company, St Louis, Missouri.Google Scholar
  53. Ressler, K. J., Sullivan, S. L., and Buck, L. B. (1993). A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73: 597–609.PubMedCrossRefGoogle Scholar
  54. Ressler, K. J., Sullivan, S. L., and Buck, L. B. (1994). Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79: 1245–1255.PubMedCrossRefGoogle Scholar
  55. Ridgway, S. H., Demski, L. S., Bullock, T. H., and Schwanzel-Fukuda, M. (1987). The terminal nerve in odontocete cetaceans. Ann. N. Y. Acad. Sci. 519: 184–200.Google Scholar
  56. Rouquier, S., Blancher, A., and Giorgi, D. (2000). The olfactory receptor gene repertoire in primates and mouse: Evidence for reduction of the functional fraction in primates. Proc. Natl. Acad. Sci. U.S.A. 97: 2870–2874.PubMedCrossRefGoogle Scholar
  57. Rowe, T. (1986). Homology and evolution of the deep dorsal thigh musculature in birds and other Reptilia. J. Morphol. 198: 327–346.Google Scholar
  58. Rowe, T. (1988). Definition, diagnosis and origin of Mammalia. J. Vertebr. Paleontol. 8: 241–264.Google Scholar
  59. Rowe, T. (1993). Phylogenetic systematics and the early history of mammals. In: Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 129–145, Springer-Verlag, New York.Google Scholar
  60. Rowe, T. (1996a). Coevolution of the mammalian middle ear and neocortex. Science 273: 651–654.Google Scholar
  61. Rowe, T. (1996b). Brain heterochrony and evolution of the mammalian middle ear. In: New Perspectives on the History of Life, M. Ghiselin and G. Pinna, eds., pp. 71–96, California Academy of Sciences, Memoir 20.Google Scholar
  62. Rowe, T. (2004). Chordate phylogeny and development. In: Assembling the Tree of Life, M. J. Donoghue and J. Cracraft, eds., pp. 384–409, Oxford University Press, Oxford.Google Scholar
  63. Rowe, T., Carlson, W., and Bottorff, W. (1993). Thrinaxodon: Digital Atlas of the Skull, CD-ROM, First edition, for MS-DOS platform, 623 megabytes, University of Texas Press, Austin, Texas.Google Scholar
  64. Rowe, T., Carlson, W., and Bottorff, W. (1995). Thrinaxodon: Digital Atlas of the Skull, CD-ROM, 2nd Ed., for Windows and Macintosh platforms, 547 megabytes, University of Texas Press, Austin, Texas.Google Scholar
  65. Rowe, T., Kappelman, J., Carlson, W. D., Ketcham, R. A., and Denison, C. (1997). High-resolution computed tomography: A breakthrough technology for Earth scientists. Geotimes 42: 23–27.Google Scholar
  66. Rowe, T., Brochu, C. A., Kishi, K., Colbert, M., and Merck, J. W. (1999). Introduction to Alligator: Digital atlas of the skull. In: Cranial Morphology of Alligator and Phylogeny of Alligatoroidae, T. Rowe, C. A. Brochu, and K. Kishi, eds., pp. 1–8, Society of Vertebrate Paleontology Memoir 6, J. Vert. Paleontol. 19, Supplement to issue 2.Google Scholar
  67. Rubin, B. D., and Katz, L. C. (1999). Cortical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23: 499–511.PubMedCrossRefGoogle Scholar
  68. Salazar, I., Quintiero, P. S., Cifuentes, J. M., Fernandez, P., and Lombardero, M. (1997). Distribution of the arterial supply to the vomeronasal organ in the cat. Anat. Rec. 247: 129–136.PubMedCrossRefGoogle Scholar
  69. Sànchez-Villagra, M. (2001). Ontogenetic and phylogenetic transformations of the vomeronasal complex and nasal floor elements in marsupial mammals. Zool. J. Linn. Soc. 131: 459–479.Google Scholar
  70. Schmidt-Nielsen, K., Hainworth, F. R., and Murrish, D. F. (1970). Counter-current exchange in the respiratory passages: Effect on water and heat balance. Respir. Physiol. 9: 263–276.PubMedCrossRefGoogle Scholar
  71. Shapiro, L. S., Roland, R. M., and Haplern, M. (1997). Development of olfactory marker protein and N_CAM expression in chemosensory systems of the opossum Monodelphis domestica. J. Morphol. 234: 109–129.PubMedCrossRefGoogle Scholar
  72. Shipley, M. T., McLean, J. H., and Ennis, M. (1995). Olfactory System. In: The Rat Nervous System, 2nd Ed., G. Paxinos, ed., pp. 899–926, Academic Press, New York.Google Scholar
  73. Singer, A. G., Agosta, W. C., Clancy, A. N., and Macrides, F. (1987). The chemistry of vomeronasally detected pheromones: Characterization of an aphrodisiac protein. Ann. N. Y. Acad. Sci. 519: 287–298.PubMedGoogle Scholar
  74. Stoddart, D. M. (ed.). (1980a). Olfaction in Mammals, Zoological Society of London, Symposium 45. Academic Press, London.Google Scholar
  75. Stoddart, D. M. (1980b). The Ecology of Vertebrate Olfaction. Chapman and Hall, London.Google Scholar
  76. Toeplitz, C. (1920). Bau und entwicklung des Knorpelschädels von Didelphys marsupialis. Zoologica 27: 1–84.Google Scholar
  77. Touhara, K., Sengoku, S., Inaki, K., Tsuboi, A., Hirono, J., Sato, T., Sakano, H., and Haga, T. (1999). Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. U.S.A. 96: 4040–4045.PubMedCrossRefGoogle Scholar
  78. VandeBerg, J. L. (1990). The gray short-tailed opossum (Monodelphis domestica) as a model didelphid species for genetic research. Austral. J. Zool. 37: 235–247.Google Scholar
  79. Van Valkenburgh, B., Theodor, J., Friscia, A., Pollack, A., and Rowe, T. (2004). Respiratory turbinates of canids and felids: A quantitative comparison. J. Zool. Lond. 264: 1–13.Google Scholar
  80. Voss, R. S., and Jansa, S. A. (2003). Phylogenetic studies on didelphid marsupials II. Nonmolecular data and new IRBP sequences: Separate and combined analyses of didelphine relationships with denser taxon sampling. Bull. Am. Mus. Nat. Hist. 276: 1–82.Google Scholar
  81. Watson, L. (1999). Jacobson's Organ, Penguin Press, London.Google Scholar
  82. Wible, J. R. (1991). Origin of Mammalia: The craniodental evidence reexamined. J. Vertebr. Paleontol. 11: 1–28.CrossRefGoogle Scholar
  83. Wible, J. R. (2003). On the cranial osteology of the short tailed opossum Monodelphis brevicaudata (Didelphidae, Marsupialia). Ann. Carneg. Mus. 72: 137–202.Google Scholar
  84. Wirsig, C. R., and Leonard, C. M. (1987). Terminal nerve damage impairs the mating-behavior of the male hamster. Brain Res. 417: 293–303.PubMedCrossRefGoogle Scholar
  85. Witmer, L. M. (1995). Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. J. Morphol. 225: 269–327.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Timothy B. Rowe
    • 1
    • 2
    • 3
  • Thomas P. Eiting
    • 1
  • Thomas E. Macrini
    • 1
  • Richard A. Ketcham
    • 1
  1. 1.Jackson School of GeosciencesThe University of Texas at AustinAustinUSA
  2. 2.Texas Memorial MuseumThe University of Texas at AustinAustinUSA
  3. 3.Geol. Science DepartmentThe University of Texas at AustinAustinUSA

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