Monodelphis domestica, the gray short-tailed opossum, is native to Brazil, Bolivia, Paraguay, and Argentina, but has found its way to North America as a common biomedical laboratory test animal. Monodelphis is a member of Didelphidae, a group of exclusively New World opossums thought to be basal among the living marsupials.

Didelphids are often used to approximate basal mammals because they retain several osteological features considered primitive for Mammalia, and are characterized by relatively few derived characters. Within Didelphidae, Monodelphis is most closely related a clade of small-bodied taxa including Marmosa, the mouse opossum. A more familiar and more distant cousin of M. domestica is the Virginia opossum, Didelphis virginiana. These two taxa are distinguishable in a number of ways: Monodelphis is approximately 50 times smaller in body size than Didelphis, and lacks a pouch which is found in the latter. Furthermore, the skulls of the two opossums vary in several ways (see Macrini, 2000).

Development in marsupials is of particular interest because many of the features that originate embryonically in placental mammals do not appear until after birth in marsupials. Thus, development of systems such as the skeleton are easier to study in marsupials making growth series such as this one invaluable to the study of mammalian evolution, and the relationship between ontogeny and phylogeny (Clark and Smith, 1993; Macrini, 2000).

Monodelphis is an excellent taxon to study postnatal development of the mammalian skeleton because the young are born 14 days after conception. At birth (day 0 in the growth series), very little of the skeleton is ossified -- only portions of the dentary. The growth series scanned and displayed here ranges from day 27 postnatal to an adult (usually older than day 120, based on its fully erupted dentition).

Several features of mammalian development are visible in members of the growth series shown on this website. An obvious change is the thickening of the skull elements as ontogeny progresses -- particularly the bones that surround the braincase and the ear region (contrast the thickness of the bones in the unreduced coronal slice #401 in day 27 and the unreduced coronal slice #390 in day 90, shown below). A feature associated with the thickening of the skull bones is the closure of the parietal fontenelle between days 48 and 57.

Another notable feature is the reduction in size of the petrosals relative to the rest of the braincase through ontogeny. This is due to changes in the size and shape of the braincase relative to the petrosal size, which remains fairly constant in size throughout postnatal ontogeny. Also, the eruption of the dentition can easily be studied from the CT scans, including the marsupial replacement pattern of the deciduous third premolar only. Events not well described in mammalian development, such as the relationship of the mental foramen to the roots of the erupting and replacing dentition, can be examined in detail using the CT imagery (see Macrini, 2000 for a description of this relationship in the adult Monodelphis).

A skull from an adult female Monodelphis domestica was CT scanned for this project. This specimen, obtained from the Southwest Foundation for Biomedical Research (SFBR) in San Antonio, Texas, where it was used as a test animal for cancer research. It lived its entire life in captivity and consequently, accurate ontogenetic and sex data are available for this specimen. Currently, this skull along with the complete postcranial skeleton belongs to the Texas Memorial Museum (TMM) recent mammals collections (TMM M-7599) housed at the Vertebrate Paleontology Laboratory in Austin, TX.

Dorsal view of the skull of Monodelphis domestica, TMM M-7599. Scale is in cm.	Ventral view of the skull of Monodelphis domestica, TMM M-7599. Scale is in cm.
The lower jaw of Monodelphis domestica, TMM M-7599. Scale is in cm.

The skull was digitally sliced using the high resolution X-ray computed tomography (CT) scanner at the University of Texas High Resolution X-ray CT Facility in Austin, Texas on 15 April 1998 by Cambria Denison and Timothy Rowe. The specimen was CT sliced in the coronal plane at a 190% offset from horizontal, without a filter, in an air wedge with a slice thickness of 0.095 mm and an interslice spacing of 0.09 mm, the space between consecutive slices. The "S.O.D.", source-object distance, the distance between the X-ray generation point and the specimen, was 40 mm. Electrons from the filament, the source of electrons, set at 0.299 mA were accelerated through a potential of 80 kV. Two-dimensional slices were reconstructed from X-rays using the following parameters: field of reconstruction 23 mm, reconstruction offset 0, reconstruction scale 15. For each slice, black color values represent air and white values represent bone. Images, output by the scanner were 12 bit, 512x512 size TIFF file format images. These files were converted to 8bit and 16bit size files in Adobe Photoshop 4.0. Tonal contrasts were adjusted on the 16 bit images in Photoshop to maximize the image contrast. The slices were then reduced to 8 bit files in Photoshop and then stacked and resliced in two orthogonal planes (sagittal and horizontal) in NIH Image 1.62b17_ppc. These images were then reduced to a maximum width of 320 pixels in Photoshop and numbered in NIH Image. The animations were created in MoviePlayer from the 320 pixel width TIFF images.

Literature

Archer, M. 1976. The basicranial region of marsupicarnivores (Marsupialia), interrelationships of carnivorous marsupials, and the affinities of the insectivorous marsupial peramelids. Zoological Journal of the Linnean Society 59:217-322.

Broom, R. 1909. Observations on the development of the marsupial skull. Proceeding of the Linnean Society of New South Wales 34:195-214.

Clark, C. T., and K. K. Smith. 1993. Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). Journal of Morphology 215:119-149.

de Beer, G. 1937. The development of the vertebrate skull. Clarendon Press, Oxford, 552pp.

Evans, H. E. 1993. Miller's anatomy of the dog. 3rd edition. Philadelphia: W. B. Saunders Company, 1113 pp.

Filan, S. 1991. Development of the middle ear region in Monodelphis domestica (Marsupialia, Didelphidae): marsupial solutions to an early birth. Journal of Zoology (London) 225:577-588.

Gray, H. 1977. Anatomy, descriptive and surgical. 15th edition. New York: Crown Publishers, INC., 1257 pp.

Kemp, T. S. 1982. Mammal-like reptiles and the origin of mammals. Academic Press, New York, 363 pp.

Larsell, O., E. McCrady, Jr., and A. A. Zimmermann. 1935. Morphological and functional development of the membraneous labyrinth in the opossum. Journal of Comparative Neurology 63:95-118.

MacIntyre, G. T. 1972. The trisulcate petrosal pattern of mammals. In: T. Dobzhansky, M. K. Hecht, and W. C. Steere (eds.), Evolutionary biology. Vol. 6. Appleton-Century-Crofts, New York, pp. 275-303.

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, University of Texas, Austin, Texas, 158 pp.

Macrini, T. E. 2004. Monodelphis domestica. Mammalian Species 760:1-8.

Maier, W. 1987. The ontogenetic development of the orbitotemporal region of the skull of Monodelphis domestica (Didelphidae, Marsupialia), and the problem of the mammalian alisphenoid. In: H. J. Kuhn and U. Zeller (eds.), Mammalia depicta, morphogenesis of the mammalian skull. Paul Parey Verlag, Hamburg, pp. 71-90.

________. 1987. Der processus angularis bei Monodelphis domestica (Didelphidae; Marsupialia) und seine beziehungen zum mittelohr: eine ontogenetische und evolutionmorphologische untersuchung. Gegenbaurs morphologisches Jahrbuch 133:123-161.

Meng, J., and R. C. Fox. 1995. Osseous inner ear structures and hearing in early marsupials and placentals. Zoological Journal of the Linnean Society 115:47-71.

McClain, J. A. 1939. The development of the auditory ossicles of the opossum (Didelphis virginiana). Journal of Morphology 64:211-265.

Murray, P., R. Wells, and M. Plane. 1987. The cranium of the Miocene thylacoleonid, Wakaleo vanderleuri: go to the shears- a fresh bite at thylacoleonid systematics. In: M. Archer (ed.), Possums and opossums: studies in evolution. Vol. 2. Surrey Beatty and Sons Pty Limited, Sydney, pp. 433-466.

Negus, V. 1958. The comparative anatomy and physiology of the nose and paranasal sinuses. E. S. Livingstone Ltd., London, 402 pp.

Novacek, M. J. 1993. Patterns of diversity in the mammalian skull. In: J. Hanken and B. K. Hull (eds.), The skull: patterns of structural and systematic diversity. Vol. 2. University of Chicago Press, Chicago, pp.438-545.

Reig, O. A., J. A. W. Kirsch, and L. G. Marshall. 1987. Systematic relationships of the living and Neocenozoic American "opossum-like" marsupials (Suborder Didelphimorphia), with comment on the classification of these and of the Cretaceous and Paleogene new world and European Metatherians. In: M. Archer (ed.), Possums and opossums: studies in evolution. Vol. 1. Surrey Beatty and Sons Pty Limited, Sydney, pp. 1-89.

Rowe, T. 1996. Brain heterochrony and the origin of the mammalian middle ear. Memoirs of the California Academy of Sciences 20:71-95.

_______, W. Carlson, and W. Bottorff. 1993. Thrinaxodon: digital atlas of the skull. University of Texas Press, Austin (2nd edition, CD-ROM for MS Windows/ Macintosh platforms).

Smith, K. K. 1994. Development of the craniofacial musculature in Monodelphis domestica (Marsupialia, Didelphidae). Journal of Morphology 222:149-173.

Weil, R. 1899. Development of the ossicula audita in the opossum. Annals of the New York Academy of Sciences 12:103-113.

Wible, J. R. 1990. Petrosals of late Cretaceous marsupials from North America, and a cladistic analysis of the petrosal in therian mammals. Journal of Vertebrate Paleontology 10:183-205.

_________, and J. A. Hopson. 1993. Basicranial evidence for early mammal phylogeny. In: F. S. Szalay, M. J. Novacek, M. C. McKenna (eds.), Mammal phylogeny: Mesozoic differentiation, multituberculates, monotremes, early therians, and marsupials. Vol. 1. Springer-Verlag, New York, pp. 45-62.

Links

Southwest Foundation for Biomedical Research

The National Opossum Society

Didelphis virginiana on The Animal Diversity Web (The University of Michigan Museum of Zoology)

The brain of Didelphis virginiana (Comparative Mammalian Brain Collections website)

Didelphis virginiana on The Mammals of Texas Online Edition

Sakaguchi Lab (Iowa State University)

Smith Lab (Duke University)

Segmented skull movie showing the individual elements of the skull. Click on thumbnail to view movie.	Horizontal slice movies through homologous points showing differences between Monodelphis (left) and Thrinaxodon (right). Click on thumbnail to view movie.

Roll spin isosurface movie showing the cranial endocast with the skull rendered somewhat transparent. Click on thumbnail to view movie.	Roll spin isosurface movie showing the cranial endocast only. Click on thumbnail to view movie.

Imagery below for Rowe et al. (in review) Organization of the olfactory and repiratory skeleton in the nose of the gray short-tailed opossum Monodelphis domestica. Journal of Mammalian Evolution

This is an animation through the skull of Monodelphis domestica. The olfactory and respiratory turbinals are colored on one side.	Figure 1. Left lateral view of the skull.

Figure 2. Views of the skull, showing the approximate locations of CT images in three orthogonal planes.	Figure 3. Dorsal view of skull with the braincase roof removed.	Figure 4. Skull with a portion of the palate removed.

Figure 5. Serial sections through the head of a 10-day-old individual.	Figure 6. Views of the respiratory chamber and olfactory passage.	Figure 7. Coronal CT slices through the skull.

Figure 8. More coronal CT images through the skull.	Figure 9. Sagittal CT images through the skull.	Figure 10. Horizontal CT images through the skull.

Figure 11. Views of endoturbinals I, II, and III.	Figure 12. Views of endoturbinals IV and V and the maxilloturbinal.	Figure 13. Views of the two ectoturbinals and the nasoturbinal.

VRML of the crescent-shaped portion of endoturbinal I. See Fig. 11a, b.	VRML of the portion of endoturbinal I bounding the maxillary sinus.	VRML of the remainder of endoturbinal I.

VRML of endoturbinal II.	VRML of endoturbinal III.	VRML of endoturbinal IV.

VRML of endoturbinal V.	VRML of the maxilloturbinal.	VRML of the majority of the nasoturbinal.

VRML of the remnant dorsal portion of the nasoturbinal after endoturbinal I arises and splits the nasoturbinal posteriorly in the nose.	VRML of the cavity occupied by the nasal gland.	VRML of the respiratory passageway.

VRML of the olfactory passageway.	VRML of ectoturbinal I.	VRML of of ectoturbinal II.