Skip to main content

Advertisement

SpringerLink
Log in

Origin of the Lateral Wall of the Mammalian Skull: Fossils, Monotremes and Therians Revisited

  • Original Paper
  • Published:
Journal of Mammalian Evolution Aims and scope Submit manuscript

Abstract

To interpret the fundamental differences in the structure and origin of the braincase sidewalls of monotremes, multituberculates, and therians, we examined MicroCT scans of a mammaliaform, Morganucodon; two non-mammalian cynodonts, Massetognathus and Probainognathus; a stem therian, Vincelestes; a juvenile and adult monotreme, Ornithorhynchus; and two marsupials, Monodelphis and Didelphis. The skull of Morganucodon resembles the pattern predicted for an early mammal: the descending flanges of the frontal and parietal cover the lateral surface of the orbitosphenoid and the palatine forms most of the medial wall of the orbit. In monotremes, the lateral region of the chondrocranium ossifies to form a long presphenoid/orbitosphenoid complex. During the transition from early mammals to extant mammals the height of the alisphenoid decreased drastically, the anterior lamina extended anteriorly to form part of the sidewall while the lateral surface of the orbitosphenoid was exposed by the dorsal withdrawal of the frontal and parietal. By contrast, in multituberculates and therians the lateral edges of the frontals extended further ventrally and the orbitosphenoid was reduced to a smaller orbital exposure below the frontals. In multituberculates the alisphenoid decreased in height, replaced by an anterior extension of the anterior lamina. The palatine withdrew from the orbital wall, replaced by a dorsally directed expansion of the maxilla. Extant therians have lost the anterior lamina. The inferior edges of the frontal followed the further ventral migration of the orbitosphenoid. The alisphenoid and parietal form most of the braincase sidewall.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdala F, Jashashvili T, Rubidge BS, Van Den Heever J (2014) New material of Microgomphodon oligocynus (Eutherapsida, Therocephalia) and the taxonomy of southern African Bauriidae. In: Kammerer CF, Angielczyk KD, Frobisch J (eds) Early Evolutionary History of the Synapsida. Springer, Dordrecht, pp 209–231

  • Averianov AO, Lopatin AV (2014) On the phylogenetic position of monotremes (Mammalia, Monotremata). Paleontol J 48(4):426–446

    Article  Google Scholar 

  • Bellairs ADA, Kamal AM (1981) The chondocranium and the development of the skull in recent reptiles. In: Gans C, Parsons TS (eds) Biology of the Reptilia: Morphology F. Academic Press, Toronto, 11, pp 1–263

    Google Scholar 

  • Bemmelen JFV (1901) Der Schadelbau der Monotremen. Denkschr med-naturw Ges Jena VI:729-798

  • Bonaparte JF (1962) Descripcion del craneo y mandibula de Exaeretodon frenguelli, Cabrera y su comparacion con Diademodontidae, Tritylodontidae y los Cinodontes sudamericanos. Publ Mus Municip Cienc Nat Mar del Plata 1:135–202

    Google Scholar 

  • Bonaparte JF, Migale LA (2010) Protomamíferos y mamíferos mesozoicos de América del Sur. Museo Municipal de Ciencias Naturales Carlos Amgehino, Buenos Aires

    Google Scholar 

  • Bonaparte JF, Soares MB, Martinelli AG (2012) Discoveries in the Late Triassic of Brazil improve knowledge on the origin of mammals. Hist Nat (Corr) 2(2):5–30

  • Brusatte S, Luo Z-X (2016) The ascent of mammals. Sci Am 314:28–35

    Article  PubMed  Google Scholar 

  • Clark CT, Smith KK (1993) Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J Morphol 215(2):119–149

    Article  PubMed  CAS  Google Scholar 

  • Crompton AW (1958) The cranial morphology of a new genus and species of ictidosauran. Proc Zool Soc London 130(2):183–216

    Article  Google Scholar 

  • Crompton AW, Jenkins FA Jr (1979) Origin of mammals. In: Lillegraven JA, Kielan-Jaworowska Z, Clemens WA (eds) Mesozoic Mammals: The First Two-thirds of Mammalian History. University of California Press, Berkeley, Los Angeles & London, pp 59–73

  • Crompton AW, Luo Z (1993) Relationships of the Liassic mammals Sinoconodon, Morganucodon oehleri, and Dinnetherium. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials. Springer-Verlag, New York, pp 30–44

  • De Beer GR (1937) The Development of the Vertebrate Skull. Clarendon Press, Oxford

  • De Beer GR (1985) The Development of the Vertebrate Skull. The University of Chicago Press, Chicago

  • De Beer GR, Fell WA (1936) The development of Monotremata. Part III. The development of the skull of Ornithorhynchus. Trans Zool Soc London 28:1–42

    Google Scholar 

  • Gambaryan PP, Kielan-Jaworowska Z (1995) Masticatory musculature of Asian taeniolabidoid multituberculate mammals. Acta Palaeontol Pol 40(1):45–108

    Google Scholar 

  • Goodrich ES (1930) Studies on the Structure and Development of Vertebrates. Macmillan and co., limited, London

  • Griffiths M (1978) The Biology of the Monotremes. Academic Press, New York

    Google Scholar 

  • Hopson JA (1964) The braincase of the advanced mammal-like reptile Bienotherium. Postilla 87:1–30

  • Hopson JA, Rougier GW (1993) Braincase structure in the oldest known skull of a therian mammal: implications for mammalian systematics and cranial evolution. Am J Sci 293:268–299

  • Huttenlocker AK, Abdala F (2015) Revision of the first therocephalian, Theriognathus owen (Therapsida: Whaitsiidae), and implications for cranial ontogeny and allometry in nonmammaliaform eutheriodonts. J Paleontol 89(4):645–664

    Article  Google Scholar 

  • Kemp TS (1972) Whaitsiid Therocephalia and the origin of cynodonts. Philos Trans R Soc Lond Ser B Biol Sci 264(857):1–53

    Article  Google Scholar 

  • Kemp TS (2009) The endocranial cavity of a nonmammalian eucynodont, Chiniquodon theotenicus, and its implications for the origin of the mammalian brain. J Vertebr Paleontol 29(4):1188–1198

    Article  Google Scholar 

  • Kermack KA (1963) The cranial structure of the triconodonts. Philos Trans R Soc Lond Ser B Biol Sci 248B:83–103

    Article  Google Scholar 

  • Kermack KA, Kielan-Jaworowska Z (1971) Therian and non-therian mammals. In: Kermack DM, Kermack KA (eds) Early Mammals. Academic Press, London, pp 103–115

  • Kermack KA, Musset F, Rigney HW (1981) The skull of Morganucodon. Zool J Linn Soc 71(1):1–158

  • Kesteven HL, Furst HC (1929) The skull of Ornithorhynchus, its later development and adult stages. J Anat 63:447–472

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure. Columbia University Press, New York

  • Kielan-Jaworowska Z, Crompton AW, Jenkins FA Jr (1987) The origin of egg-laying mammals. Nature 326(6116):871–873

  • Kuhn HJ, Zeller U (1987) The cavum epiptericum in monotremes and therian mammals. In: Kuhn HJ, Zeller U (eds) Morphogenesis of the Mammalian Skull. Mammalia Depicta. Verlag Paul Parey, Hamburg and Berlin, pp 51–70

  • Liu J, Olsen P (2010) The phylogenetic relationships of Eucynodontia (Amniota: Synapsida). J Mammal Evol 17(3):151–176

  • Luo Z-X (2007) Transformation and diversification in early mammal evolution. Nature 450(7172):1011–1019

    Article  PubMed  CAS  Google Scholar 

  • Luo Z-X, Cifelli RL, Kielan-Jaworowska Z (2001) Dual origin of tribosphenic mammals. Nature 409(6816):53–57

    Article  PubMed  CAS  Google Scholar 

  • Luo Z-X, Gatesy SM, Jenkins FA Jr, Amaral WW, Shubin NH (2015) Mandibular and dental characteristics of Late Triassic mammaliaform Haramiyavia and their ramifications for basal mammal evolution. Proc Natl Acad Sci U S A 112(51):E7101-E7109

  • Luo Z-X, Kielan-Jaworowska Z, Cifelli RL (2002) In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol Pol 47(1):1–78

    Google Scholar 

  • Macrini TE, Rougier GW, Rowe T (2007) Description of a cranial endocast from the fossil mammal Vincelestes neuquenianus (Theriiformes) and its relevance to the evolution of endocranial characters in therians. Anat Rec Adv Integr Anat Evol Biol 290(7):875–892

    Article  Google Scholar 

  • Maier W (1987) The ontogenetic development of the orbitotemporal region in the skull of Monodelphis domestica (Didelphidae, Marsupialia), and the problem of the mammalian alisphenoid. In: Kuhn HJ, Zeller U (eds) Morphogenesis of the Mammalian Skull. Mammalia Depicta. Verlag Paul Parey, Hamburg and Berlin, pp 71–90

  • Martinelli AG, Bento Soares M (2016) Evolution of South American non-mammaliaform cynodonts (Therapsida, Cynodontia). In: Agnolin FL, Lio GL, Egli FB, Chimento NR, Novas FE (eds) Contribuciones del MACN: Historia Evolutiva y Paleobiogeográfica de los Vertebrados de América del Sur. Buenos Aires, 6, pp 183–196

  • Martinelli AG, De La Fuente M, Abdala F (2009) Diademodon tetragonus Seeley, 1894 (Therapsida: Cynodontia) in the Triassic of South America and its biostratigraphic implications. J Vertebr Paleontol 29(3):852–862

    Article  Google Scholar 

  • Martinelli AG, Rougier GW (2007) On Chaliminia musteloides (Eucynodontia: Tritheledontidae) from the Late Triassic of Argentina, and a phylogeny of Ictidosauria. J Vertebr Paleontol 27(2):442–460

  • Mcbratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322(1):121–132

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meng J, Bi S, Zheng X, Wang X (2016) Ear ossicle morphology of the Jurassic euharamiyidan Arboroharamiya and evolution of mammalian middle ear. J Morphol doi: 10.1002/jmor.20565

  • Miao D (1988) Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata) and its implications to mammalian evolution. Contrib Geol Univ Wyoming Spec Pap 4:1–104

    Google Scholar 

  • Miller ME, Christiansen GC, Evans HE (1964) Anatomy of the Dog. W.B. Saunders, Philadelphia

  • Moore WJ (1981) The Mammalian Skull. Cambridge University Press, Cambridge

  • Musser AM, Archer M (1998) New information about the skull and dentary of the Miocene platypus Obdurodon dicksoni, and a discussion of ornithorhynchid relationships. Philos Trans R Soc Lond B Biol Sci 353(1372):1063–1079

  • Pascual R, Goin FJ, Balarino L, Sauthier DEU (2002) New data on the Paleocene monotreme Monotrematum sudamericanum, and the convergent evolution of triangulate molars. Acta Palaeontol Pol 47(3):487–492

    Google Scholar 

  • Presley R (1981) Alisphenoid equivalents in placentals, marsupials, monotremes and fossils. Nature 294(5842):668–670

    Article  Google Scholar 

  • Presley R, Steel FLD (1976) On the homology of the alisphenoid. J Anat 121(3):441–459

    Google Scholar 

  • Quiroga JC (1979) The brain of two mammal-like reptiles (Cynodontia - Therapsida). J Hirnforsch 20(4):341–350

    PubMed  CAS  Google Scholar 

  • Quiroga JC (1984) The endocranial cast of the advanced mammal-like reptile Therioherpeton cargnini (Therapsida, Cynodontia) from the Middle Triassic of Brazil. J Hirnforsch 25(3):285–290

  • Rich TH, Hopson JA, Gill PG, Trusler P, Rogers-Davidson S, Morton S, Cifelli RL, Pickering D, Kool L, Siu K, Burgmann FA, Senden T, Evans AR, Wagstaff BE, Seegets-Villiers D, Corfe IJ, Flannery TF, Walker K, Musser AM, Archer M, Pian R, Vickers-Rich P (2016) The mandible and dentition of the Early Cretaceous monotreme Teinolophos trusleri. Alcheringa: 40:1–27

  • Rich TH, Piper KJ, Pickering D, Wright S (2006) Further Ektopodontidae (Phalangeroidea, Mammalia) from southwestern Victoria. Alcheringa 30(1):133–140

    Article  Google Scholar 

  • Rich TH, Vickers-Rich P, Constantine A, Flannery TF, Kool L, Van Klaveren N (1997) A tribosphenic mammal from the Mesozoic of Australia. Science 278(5342):1438–1442

    Article  PubMed  CAS  Google Scholar 

  • Rich TH, Vickers-Rich P, Trusler P, Flannery TF, Cifelli R, Constantine A, Kool L, Van Klaveren N (2001) Monotreme nature of the Australian Early Cretaceous mammal Teinolophos. Acta Palaeontol Pol 46(1):113–118

  • Rodrigues PG, Ruf I, Schultz CL (2013) Digital reconstruction of the otic region and inner ear of the non-mammalian cynodont Brasilitherium riograndensis (Late Triassic, Brazil) and its relevance to the evolution of the mammalian ear. J Mammal Evol 20(4):291–307

  • Rougier GW, Martinelli AG, Forasiepi AM, Novacek MJ (2007) New Jurassic mammals from Patagonia, Argentina: a reappraisal of australosphenidan morphology and interrelationships. Am Mus Novitates 3566:1–54

  • Rougier GW, Wible JR, Novacek MJ (2004) New specimen of Deltatheroides cretacicus (Metatheria, Deltatheroida) from the Late Cretaceous of Mongolia. Bull Carnegie Mus Nat Hist 36:245–266

  • Rowe T (1986) Osteological diagnosis of Mammalia, L.1758, and its relationship to extinct Synapsida. PhD dissertation, University of California, Berkeley

  • Rowe T (1987) Definition and diagnosis in the phylogenetic system. Syst Zool 36(2):208–211

    Article  Google Scholar 

  • Rowe T (1988) Definition, diagnosis, and origin of Mammalia. J Vertebr Paleontol 8(3):241–264

    Article  Google Scholar 

  • Rowe T (1993) Phylogenetic systematics and the early history of mammals. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials. Springer-Verlag, New York, pp 129–145

  • Rowe TB, Eiting TP, Macrini TE, Ketcham RA (2005) Organization of the olfactory and respiratory skeleton in the nose of the gray short-tailed opossum Monodelphis domestica. J Mammal Evol 12(3–4):303–336

  • Rowe TB, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):958–960

    Article  CAS  Google Scholar 

  • Rowe TB, Rich TH, Vickers-Rich P, Springer M, Woodburne MO (2008) The oldest platypus and its bearing on divergence timing of the platypus and echidna clades. Proc Natl Acad Sci U S A 105(4):1238–1242

    Article  PubMed  PubMed Central  Google Scholar 

  • Sidor CA, Hancox PJ (2006) Elliotherium kersteni, a new tritheledontid from the lower Elliot Formation (Upper Triassic) of South Africa. J Paleontol 80(2):333–342

  • Starck D (1967) Le crâne des mammifères. In: Grassé PP (ed) Traité de Zoologie, Anatomie, Systématique, Biologie. Masson, Paris, Tome XVI, Fascicule 1, pp 405–549

  • Sues H-D (1986) The skull and dentition of two tritylodontid synapsids from the Lower Jurassic of western North America. Bull Mus Comp Zool 151(4):217–268

  • Wible JR (2003) On the cranial osteology of the short-tailed opossum Monodelphis brevicaudata (Didelphidae, Marsupialia). Ann Carnegie Museum 72(3):137–202

    Google Scholar 

  • Wible JR, Hopson JA (1993) Basicranial evidence for early mammal phylogeny. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal Phylogeny: Mesozoic Differentiation, Multituberculates, Monotremes, Early Therians and Marsupials. Springer-Verlag, New York, pp 45–62

  • Wible JR, Rougier GW (2000) Cranial anatomy of Kryptobaatar dashzevegi (Mammalia, Multituberculata), and its bearing on the evolution of mammalian characters. Bull Am Mus Nat Hist 247:1–124

    Article  Google Scholar 

  • Zeller U (1987) Morphogenesis of the mammalian skull with special reference to Tupaia. In: Kuhn HJ, Zeller U (eds) Morphogenesis of the Mammalian Skull. Mammalia Depicta. Verlag Paul Parey, Hamburg and Berlin, pp 17–50

  • Zeller U (1989) Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abh senckenb naturforsch Ges 545:1–138

  • Zhou C-F, Wu S, Martin T, Luo Z-X (2013) A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500(7461):163–167

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to the Museum of Comparative Zoology and the Department of Organismic and Evolutionary Biology at Harvard for their support.

Author information

Authors and Affiliations

  1. Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

    A.W. Crompton & C. Musinsky

  2. Department of Anatomical Sciences & Neurobiology, University of Louisville, 511 South Floyd St, Louisville, KY, 40202, USA

    G.W. Rougier

  3. Department of Geology & Geophysics, Yale University, P.O. Box 208109, New Haven, CT, 06520-8109, USA

    B.-A.S. Bhullar & J. A. Miyamae

Authors
  1. A.W. Crompton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Musinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. G.W. Rougier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B.-A.S. Bhullar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. A. Miyamae
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A.W. Crompton.

Electronic supplementary material

ESM 1

Morganucodon watsoni (IVPP 8682) a, stereo of the anterior view of the braincase, with frontals, parietals and right petrosal omitted; b, stereo of the internal view of the right side of the braincase (with bones on the left side omitted) and interpretation (PDF 3726 kb)

ESM 2

Ornithorhynchus anatinus (AMNH 2013). Stereo view of the internal view of the right side of the braincase (PDF 2267 kb)

ESM 3

Ornithorhynchus anatinus (AMNH 2013). Video showing half rotation of the orbitosphenoids (shades of pink), presphenoid (purple), palatine (mauve), mesethmoid (green), and pterygoids (yellow orange), basisphenoid (red); followed by a completion of the rotation with additional bones added: anterior lamina, squamosal and parietal (shades of blue), maxilla (yellow), dentary, frontal, supraoccipital, basioccipital, exoccipital and petrosal, (shades of green) (MP4 8052 kb)

ESM 4

Stereo photographs of Vincelestes neuquenianus (MACN-N 04). a, partial view of the left side of the braincase; b. internal view of the left side of the braincase; c, ventral view of braincase; d, dorsal view of the braincase; e, horizontal section through the braincase to illustrate the relation of the orbital flanges of the palatine to the presphenoid/orbitosphenoid (PDF 5391 kb)

ESM 5

Probainognathus jenseni (MCZ 4280). Video showing rotation of the orbitosphenoid and fragment of the frontal (MPG 40415 kb)

ESM 6

Morganucodon watsoni (IVPP 8682). Video showing rotation of segmented bones of the skull (MPG 105554 kb)

ESM 7

Vincelestes neuquenianus (MACN-N05). Video showing rotation of the orbitosphenoids/presphenoid (pink), palatines (red), mesethmoid (light blue), and pterygoids (dark red), followed by rotation of the whole skull with the left side roof and zygomatic arch removed, also partially segmented (MP4 85,647 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crompton, A., Musinsky, C., Rougier, G. et al. Origin of the Lateral Wall of the Mammalian Skull: Fossils, Monotremes and Therians Revisited. J Mammal Evol 25, 301–313 (2018). https://doi.org/10.1007/s10914-017-9388-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10914-017-9388-7

Keywords

Search

Navigation