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

  • A.W. Crompton
  • C. Musinsky
  • G.W. Rougier
  • B.-A.S. Bhullar
  • J. A. Miyamae
Original Paper

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.

Keywords

Braincase sidewall Orbitosphenoid Monotremes Ictidosaurs Morganucodon Vincelestes 

Notes

Acknowledgements

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

Supplementary material

10914_2017_9388_MOESM1_ESM.pdf (3.6 mb)
ESM 1Morganucodon 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)
10914_2017_9388_MOESM2_ESM.pdf (2.2 mb)
ESM 2Ornithorhynchus anatinus (AMNH 2013). Stereo view of the internal view of the right side of the braincase (PDF 2267 kb)
10914_2017_9388_MOESM3_ESM.mp4 (7.9 mb)
ESM 3Ornithorhynchus 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)
10914_2017_9388_MOESM4_ESM.pdf (5.3 mb)
ESM 4Stereo 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)
10914_2017_9388_MOESM5_ESM.mpg (39.5 mb)
ESM 5Probainognathus jenseni (MCZ 4280). Video showing rotation of the orbitosphenoid and fragment of the frontal (MPG 40415 kb)
10914_2017_9388_MOESM6_ESM.mpg (103.1 mb)
ESM 6Morganucodon watsoni (IVPP 8682). Video showing rotation of segmented bones of the skull (MPG 105554 kb)
10914_2017_9388_MOESM7_ESM.mp4 (83.6 mb)
ESM 7Vincelestes 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)

References

  1. 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 209–231Google Scholar
  2. Averianov AO, Lopatin AV (2014) On the phylogenetic position of monotremes (Mammalia, Monotremata). Paleontol J 48(4):426–446CrossRefGoogle Scholar
  3. 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 1–263Google Scholar
  4. Bemmelen JFV (1901) Der Schadelbau der Monotremen. Denkschr med-naturw Ges Jena VI:729-798Google Scholar
  5. 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 1:135–202Google Scholar
  6. Bonaparte JF, Migale LA (2010) Protomamíferos y mamíferos mesozoicos de América del Sur. Museo Municipal de Ciencias Naturales Carlos Amgehino, Buenos AiresGoogle Scholar
  7. 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):5–30Google Scholar
  8. Brusatte S, Luo Z-X (2016) The ascent of mammals. Sci Am 314:28–35CrossRefPubMedGoogle Scholar
  9. Clark CT, Smith KK (1993) Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J Morphol 215(2):119–149CrossRefPubMedGoogle Scholar
  10. Crompton AW (1958) The cranial morphology of a new genus and species of ictidosauran. Proc Zool Soc London 130(2):183–216CrossRefGoogle Scholar
  11. 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 59–73Google Scholar
  12. 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 30–44Google Scholar
  13. De Beer GR (1937) The Development of the Vertebrate Skull. Clarendon Press, OxfordGoogle Scholar
  14. De Beer GR (1985) The Development of the Vertebrate Skull. The University of Chicago Press, ChicagoGoogle Scholar
  15. De Beer GR, Fell WA (1936) The development of Monotremata. Part III. The development of the skull of Ornithorhynchus. Trans Zool Soc London 28:1–42Google Scholar
  16. Gambaryan PP, Kielan-Jaworowska Z (1995) Masticatory musculature of Asian taeniolabidoid multituberculate mammals. Acta Palaeontol Pol 40(1):45–108Google Scholar
  17. Goodrich ES (1930) Studies on the Structure and Development of Vertebrates. Macmillan and co., limited, LondonGoogle Scholar
  18. Griffiths M (1978) The Biology of the Monotremes. Academic Press, New YorkGoogle Scholar
  19. Hopson JA (1964) The braincase of the advanced mammal-like reptile Bienotherium. Postilla 87:1–30Google Scholar
  20. 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 293:268–299Google Scholar
  21. 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):645–664CrossRefGoogle Scholar
  22. Kemp TS (1972) Whaitsiid Therocephalia and the origin of cynodonts. Philos Trans R Soc Lond Ser B Biol Sci 264(857):1–53CrossRefGoogle Scholar
  23. 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):1188–1198CrossRefGoogle Scholar
  24. Kermack KA (1963) The cranial structure of the triconodonts. Philos Trans R Soc Lond Ser B Biol Sci 248B:83–103CrossRefGoogle Scholar
  25. Kermack KA, Kielan-Jaworowska Z (1971) Therian and non-therian mammals. In: Kermack DM, Kermack KA (eds) Early Mammals. Academic Press, London, pp 103–115Google Scholar
  26. Kermack KA, Musset F, Rigney HW (1981) The skull of Morganucodon. Zool J Linn Soc 71(1):1–158Google Scholar
  27. Kesteven HL, Furst HC (1929) The skull of Ornithorhynchus, its later development and adult stages. J Anat 63:447–472PubMedPubMedCentralGoogle Scholar
  28. Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure. Columbia University Press, New YorkGoogle Scholar
  29. Kielan-Jaworowska Z, Crompton AW, Jenkins FA Jr (1987) The origin of egg-laying mammals. Nature 326(6116):871–873Google Scholar
  30. 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 51–70Google Scholar
  31. Liu J, Olsen P (2010) The phylogenetic relationships of Eucynodontia (Amniota: Synapsida). J Mammal Evol 17(3):151–176Google Scholar
  32. Luo Z-X (2007) Transformation and diversification in early mammal evolution. Nature 450(7172):1011–1019CrossRefPubMedGoogle Scholar
  33. Luo Z-X, Cifelli RL, Kielan-Jaworowska Z (2001) Dual origin of tribosphenic mammals. Nature 409(6816):53–57CrossRefPubMedGoogle Scholar
  34. 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-E7109Google Scholar
  35. Luo Z-X, Kielan-Jaworowska Z, Cifelli RL (2002) In quest for a phylogeny of Mesozoic mammals. Acta Palaeontol Pol 47(1):1–78Google Scholar
  36. 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):875–892CrossRefGoogle Scholar
  37. 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 71–90Google Scholar
  38. 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 183–196Google Scholar
  39. 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):852–862CrossRefGoogle Scholar
  40. 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):442–460Google Scholar
  41. 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):121–132CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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
  43. Miao D (1988) Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata) and its implications to mammalian evolution. Contrib Geol Univ Wyoming Spec Pap 4:1–104Google Scholar
  44. Miller ME, Christiansen GC, Evans HE (1964) Anatomy of the Dog. W.B. Saunders, PhiladelphiaGoogle Scholar
  45. Moore WJ (1981) The Mammalian Skull. Cambridge University Press, CambridgeGoogle Scholar
  46. 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):1063–1079Google Scholar
  47. 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):487–492Google Scholar
  48. Presley R (1981) Alisphenoid equivalents in placentals, marsupials, monotremes and fossils. Nature 294(5842):668–670CrossRefGoogle Scholar
  49. Presley R, Steel FLD (1976) On the homology of the alisphenoid. J Anat 121(3):441–459Google Scholar
  50. Quiroga JC (1979) The brain of two mammal-like reptiles (Cynodontia - Therapsida). J Hirnforsch 20(4):341–350PubMedGoogle Scholar
  51. 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):285–290Google Scholar
  52. 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: 40:1–27Google Scholar
  53. Rich TH, Piper KJ, Pickering D, Wright S (2006) Further Ektopodontidae (Phalangeroidea, Mammalia) from southwestern Victoria. Alcheringa 30(1):133–140CrossRefGoogle Scholar
  54. 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):1438–1442CrossRefPubMedGoogle Scholar
  55. 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):113–118Google Scholar
  56. 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):291–307Google Scholar
  57. 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 3566:1–54Google Scholar
  58. 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 36:245–266Google Scholar
  59. Rowe T (1986) Osteological diagnosis of Mammalia, L.1758, and its relationship to extinct Synapsida. PhD dissertation, University of California, BerkeleyGoogle Scholar
  60. Rowe T (1987) Definition and diagnosis in the phylogenetic system. Syst Zool 36(2):208–211CrossRefGoogle Scholar
  61. Rowe T (1988) Definition, diagnosis, and origin of Mammalia. J Vertebr Paleontol 8(3):241–264CrossRefGoogle Scholar
  62. 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 129–145Google Scholar
  63. 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):303–336Google Scholar
  64. Rowe TB, Macrini TE, Luo Z-X (2011) Fossil evidence on origin of the mammalian brain. Science 332(6032):958–960CrossRefGoogle Scholar
  65. 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):1238–1242CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sidor CA, Hancox PJ (2006) Elliotherium kersteni, a new tritheledontid from the lower Elliot Formation (Upper Triassic) of South Africa. J Paleontol 80(2):333–342Google Scholar
  67. Starck D (1967) Le crâne des mammifères. In: Grassé PP (ed) Traité de Zoologie, Anatomie, Systématique, Biologie. Masson, Paris, Tome XVI, Fascicule 1, pp 405–549Google Scholar
  68. 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):217–268Google Scholar
  69. Wible JR (2003) On the cranial osteology of the short-tailed opossum Monodelphis brevicaudata (Didelphidae, Marsupialia). Ann Carnegie Museum 72(3):137–202Google Scholar
  70. 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 45–62Google Scholar
  71. 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 247:1–124CrossRefGoogle Scholar
  72. 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 17–50Google Scholar
  73. Zeller U (1989) Die Entwicklung und Morphologie des Schädels von Ornithorhynchus anatinus (Mammalia: Prototheria: Monotremata). Abh senckenb naturforsch Ges 545:1–138Google Scholar
  74. Zhou C-F, Wu S, Martin T, Luo Z-X (2013) A Jurassic mammaliaform and the earliest mammalian evolutionary adaptations. Nature 500(7461):163–167CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Museum of Comparative ZoologyHarvard UniversityCambridgeUSA
  2. 2.Department of Anatomical Sciences & NeurobiologyUniversity of LouisvilleLouisvilleUSA
  3. 3.Department of Geology & GeophysicsYale UniversityNew HavenUSA

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