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.
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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
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
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
Bonaparte JF, Migale LA (2010) Protomamíferos y mamíferos mesozoicos de América del Sur. Museo Municipal de Ciencias Naturales Carlos Amgehino, Buenos Aires
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
Clark CT, Smith KK (1993) Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). J Morphol 215(2):119–149
Crompton AW (1958) The cranial morphology of a new genus and species of ictidosauran. Proc Zool Soc London 130(2):183–216
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
Gambaryan PP, Kielan-Jaworowska Z (1995) Masticatory musculature of Asian taeniolabidoid multituberculate mammals. Acta Palaeontol Pol 40(1):45–108
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
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
Kemp TS (1972) Whaitsiid Therocephalia and the origin of cynodonts. Philos Trans R Soc Lond Ser B Biol Sci 264(857):1–53
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
Kermack KA (1963) The cranial structure of the triconodonts. Philos Trans R Soc Lond Ser B Biol Sci 248B:83–103
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
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
Luo Z-X, Cifelli RL, Kielan-Jaworowska Z (2001) Dual origin of tribosphenic mammals. Nature 409(6816):53–57
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
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
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
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
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
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
Presley R (1981) Alisphenoid equivalents in placentals, marsupials, monotremes and fossils. Nature 294(5842):668–670
Presley R, Steel FLD (1976) On the homology of the alisphenoid. J Anat 121(3):441–459
Quiroga JC (1979) The brain of two mammal-like reptiles (Cynodontia - Therapsida). J Hirnforsch 20(4):341–350
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
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
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
Rowe T (1988) Definition, diagnosis, and origin of Mammalia. J Vertebr Paleontol 8(3):241–264
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
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
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
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
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
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Thanks to the Museum of Comparative Zoology and the Department of Organismic and Evolutionary Biology at Harvard for their support.
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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)
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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)
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Probainognathus jenseni (MCZ 4280). Video showing rotation of the orbitosphenoid and fragment of the frontal (MPG 40415 kb)
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Morganucodon watsoni (IVPP 8682). Video showing rotation of segmented bones of the skull (MPG 105554 kb)
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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)
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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
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DOI: https://doi.org/10.1007/s10914-017-9388-7