The origin and evolution of the mammalian brain has long been the focus of scientific enquiry. Conversely, little research has focused on the palaeoneurology of the stem group of Mammaliaformes, the Permian and Triassic non-mammaliaform Therapsida (NMT). This is because the majority of the NMT have a non-ossified braincase, making the study of their endocranial cast (sometimes called the “fossil brain”) problematic. Thus, descriptions of the morphology and size of NMT endocranial casts have been based largely on approximations rather than reliable determination. Accordingly, here we use micro-CT scans of the skulls of 1 Dinocephalia and 3 Biarmosuchia, which are NMT with a fully ossified braincase and thus a complete endocast. For the first time, our work enables the accurate determination of endocranial shape and size in NMT. This study suggests that NMT brain size falls in the upper range of the reptilian and amphibian variation. Brain size in the dicynodont Kawingasaurus is equivalent to that of early Mammaliaformes, whereas the Dinocephalia show evidence of a secondary reduction of brain size. In addition, unlike other NMT in which the endocast has a tubular shape and its parts are arranged in a linear manner, the biarmosuchian endocast is strongly flexed at the level of the midbrain, creating a near right angle between the fore- and hindbrain. These data highlight an unexpected diversity of endocranial size and morphology in NMT, features that are usually considered conservative in this group.

Keywords:
Biarmosuchia, Dinocephalia, Therapsida, Encephalisation, Endothermy, Endocast
1.
Angielczyk KD, Rubidge BS, Day MO, Lin F (2016): A reevaluation of Brachyprosopus broomi and Chelydontops altidentalis, Dicynodonts (Therapsida, Anomodontia) from the Middle Permian Tapinocephalus Assemblage Zone of the Karoo Basin, South Africa. J Vert Paleontol 36:e1078342.
2.
Araújo R, Fernandez V, Polcyn MJ, Fröbisch J, Martins RMS (2017): Aspects of gorgonopsian paleobiology and evolution: insights from the basicranium, occiput, osseous labyrinth, vasculature, and neuroanatomy. PeerJ 5:e3119.
3.
Bennett AF, Ruben JA (1986): The metabolic and thermoregulatory status of therapsids; in Hotton N, MacLean PD, Roth JJ, Roth ED (eds): Ecology and Biology of Mammal-Like Reptiles. Washington, Smithsonian Institution Press, pp 207-218.
4.
Benoit J (2015): A new method of estimating brain mass through cranial capacity in extinct proboscideans to account for the non-neural tissues surrounding their brain. J Vert Paleontol 35:e991021.
5.
Benoit J, Abdala F, Manger PR, Rubidge BS (2016a): The sixth sense in mammalians forerunners: variability of the parietal foramen and the evolution of the pineal eye in South African Permo-Triassic eutheriodont therapsids. Acta Palaeontol Pol 61:777-789.
6.
Benoit J, Crumpton N, Merigeaud S, Tabuce R (2013): A memory already like an elephant? The advanced brain morphology of the last common ancestor of Afrotheria (Mammalia). Brain Behav Evol 81:154-169.
7.
Benoit J, Fernandez V, Tafforeau P, Manger PR, Rubidge BS (2016b): Cranial bosses of Choerosaurus dejageri (Therapsida, Therocephalia): earliest evidence of cranial display structures in eutheriodonts. PLoS One 11:e0161457.
8.
Benoit J, Jasinoski SC, Fernandez V, Abdala F (2017a): The mystery of a missing bone: revealing the orbitosphenoid in basal Epicynodontia (Cynodontia, Therapsida) through computed tomography. Sci Nat 104:66.
9.
Benoit J, Manger PR, Norton LA, Fernandez V, Rubidge BS (2017b): Synchrotron scanning reveals the palaeoneurology of the head-butting Moschops capensis (Therapsida, Dinocephalia). PeerJ 5:e3496.
10.
Benoit J, Manger PR, Rubidge BS (2016c): Palaeoneurological clues to the evolution of defining mammalian soft tissue traits. Sci Rep 6:25604.
11.
Boonstra LD (1968): The braincase, basicranial axis and median septum in the Dinocephalia. Ann S Afr Mus 50:195-273.
12.
Botha-Brink J, Abdala F, Chinsamy A (2012): The radiation and osteohistology of nonmammaliaform cynodonts; in Chinsamy-Turan A (ed): Forerunners of Mammals: Radiation, Histology, Biology. Bloomington, Indiana University Press, pp 223-246.
13.
Botha-Brink J, Modesto SP (2007): A mixed-age classed ‘pelycosaur' aggregation from South Africa: earliest evidence of parental care in amniotes? Proc Biol Sci 274:2829-2834.
14.
Brink AS (1955): Note on a very tiny specimen of Thrinaxodon liorhinus. Palaeontol Afr 3:73-76.
15.
Brink AS (1965): On two new specimens of Lystrosaurus-Zone cynodonts. Palaeontol Afr 9:107-122.
16.
Case EC (1907): Revision of the Pelycosauria of North America. Washington, Carnegie Institution of Washington Publications.
17.
Castanhinha R, Araújo R, Júnior LC, Angielczyk KD, Martins GG, Martins RM, Chaouiya C, Beckmann F, Wilde F (2013): Bringing dicynodonts back to life: paleobiology and anatomy of a new emydopoid genus from the Upper Permian of Mozambique. PLoS One 8:e80974.
18.
Cluver MA (1971): The cranial morphology of the Genus Lystrosaurus. Ann S Afr Mus 56:155-273.
19.
Colbert EH, Kitching JW (1981): Scaloposaurian reptiles from the Triassic of Antarctica. Am Mus Nov 2709:1-22.
20.
Crompton AW, Musinsky C, Rougier G, Bhullar BAS, Miyamae JA (2017a): Origin of the lateral wall of the mammalian skull: fossils, monotremes and therians revisited. J Mammal Evol DOI: 10.1007/s10914-017-9388-7.
21.
Crompton AW, Owerkowicz T, Bhullar BAS, Musinsky C (2017b): Structure of the nasal region of non-mammalian cynodonts and mammaliaforms: speculations on the evolution of mammalian endothermy. J Vert Paleontol 37:e1269116.
22.
Day MO, Ramezani J, Bowring SA, Sadler PM, Erwin DH, Abdala F, Rubidge BS (2015): When and how did the terrestrial mid-Permian mass extinction occur? Evidence from the tetrapod record of the Karoo Basin, South Africa. Proc Biol Sci 282:20150834.
23.
Dechaseaux C (1962): Cerveaux d'Animaux Disparus. Paris, Masson.
24.
Edinger T (1948): Evolution of the horse brain. Geol Soc Am Mem 25:1-177.
25.
Edinger T (1975): Paleoneurology 1804-1966. An annotated bibliography. Adv Anat Embryol Cel Biol 49:1-258.
26.
Fiorelli LE, Ezcurra MD, Hechenleitner EM, Argañaraz E, Taborda JR, Trotteyn MJ, von Baczko MB, Desojo JB (2013): The oldest known communal latrines provide evidence of gregarism in Triassic megaherbivores. Sci Rep 28:3348.
27.
Fröbisch J (2006): Locomotion in derived dicynodonts (Synapsida, Anomodontia): a functional analysis of the pelvic girdle and hind limb of Tetragonias njalilus. Can J Earth Sci 43:1297-1308.
28.
Fröbisch J, Reisz RR (2009): The Late Permian herbivore Suminia and the early evolution of arboreality in terrestrial vertebrate ecosystems. Proc Biol Sci 276:3611-3618.
29.
Gillooly JF, McCoy MW (2014): Brain size varies with temperature in vertebrates. PeerJ 2:e301.
30.
Gow CE (1986): The sidewall of the braincase in cynodont therapsids, and a note on the homology of the mammalian promontorium. S Afr J Zool 21:136-148.
31.
Hillenius WJ (1994): Turbinates in therapsids: evidence for late Permian origins of mammalian endothermy. Evolution 48:207-229.
32.
Hillenius WJ, Ruben JA (2004): The evolution of endothermy in terrestrial vertebrates. Who? When? Why? Physiol Biochem Zool 77:1019-1042.
33.
Hoffmann S, O'Connor PM, Kirk EC, Wible JR, Krause DW (2014): Endocranial and inner ear morphology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. J Vertebr Paleontol 34:110-136.
34.
Hopson JA (1979): Paleoneurology; in Glans C, Northcutt RG, Ulinski P (eds): Biology of the Reptilia. New York, Academic Press, pp 39-146.
35.
Hurlburt GR, Ridgely RC, Witmer LM (2013): Relative size of brain and cerebrum in tyrannosaurid dinosaurs: an analysis using brain-endocast quantitative relationships in extant alligators; in Parrish JM, Molnar RE, Currie PJ, Koppelhus EB (eds): Tyrannosaurid Paleobiology. Bloomington, Indiana University Press, pp 135-155.
36.
Ivakhnenko MF (2008): Cranial morphology and evolution of Permian Dinomorpha (Eotherapsida) of Eastern Europe. Paleontol J 42:859-995.
37.
Jasinoski S, Abdala F (2017): Aggregations and parental care in the Early Triassic basal cynodonts Galesaurus planiceps and Thrinaxodon liorhinus. PeerJ 5:e2875
38.
Jerison HJ (1973): Evolution of the Brain and Intelligence. New York, Academic Press.
39.
Jirak D, Janacek J (2017): Volume of the crocodilian brain and endocast during ontogeny. PLoS One 12:e0178491.
40.
Kemp TS (1969): On the functional morphology of the gorgonopsid skull. Philos Trans R Soc Lond B Biol Sci 256:1-83.
41.
Kemp TS (1979): The primitive cynodont Procynosuchus: functional anatomy of the skull and relationships. Philos Trans R Soc Lond B Biol Sci 285:73-122.
42.
Kemp TS (2005): The Origin and Evolution of Mammals. Oxford, Oxford University Press.
43.
Kemp TS (2009): The endocranial cavity of a nonmammalian eucynodont, Chiniquodon theotenicus, and its implications for the origin of the mammalian brain. J Vert Paleontol 29:1188-1198.
44.
Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004): Mammals from the Age of Dinosaurs - Origins, Evolution, and Structure. New York, Columbia University Press.
45.
Kitching JW, Collinson JW, Elliot DH, Colbert EH (1972): Lystrosaurus zone (Triassic) fauna from Antarctica. Science 175:524-527.
46.
Kruger A, Rubidge BS, Abdala F, Gomani Chindebvu E, Jacobs LL (2015): Lende chiweta, a new therapsid from Malawi, and its influence on burnetiamorph phylogeny and biogeography. J Vert Paleontol 35:e1008698.
47.
Laass M (2015a): Virtual reconstruction and description of the cranial endocast of Pristerodon mackayi (Therapsida, Anomodontia). J Morphol 276:1089-1099.
48.
Laass M (2015b): Bone-conduction hearing and seismic sensitivity of the late Permian anomodont Kawingasaurus fossilis. J Morphol 276:121-143.
49.
Laass M, Kaestner A (2017): Evidence for convergent evolution of a structure comparable to the mammalian neocortex in a Late Permian therapsid. J Morphol 278:1033-1057.
50.
Laass M, Kaestner A, Schillinger B (2015): Evidence for a dual origin of a neocortex in synapsids. 86th Annual Meeting of the Paläontologische Gesellschaft 2015, Landsweiler-Reden. Zentrum für Biodokumentation, vol 4, pp 38-39.
51.
Lehman JP (1961): Dicynodontia; in Piveteau JP (ed): Traité de Paléontologie, VI, Mammifères, vol 1: Origine Reptilienne Evolution. Paris, Masson et Cie, pp 287-351.
52.
Luo ZX (2007): Transformation and diversification in early mammal evolution. Nature 450:1011-1019.
53.
Manger PR (2006): An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol Rev 81:293-338.
54.
Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J (2014): The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities. Nucl Instr Meth Phys Res B 324:41-48.
55.
Nasterlack T, Canoville A, Chinsamy A (2012): New insights into the biology of the permian genus Cistecephalus (Therapsida, Dicynodontia). J Vert Paleontol 32:1396-1410.
56.
Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (1998): The Central Nervous System of Vertebrates. Berlin, Springer.
57.
Olson EC (1944): Origin of mammals based upon cranial morphology of the therapsid suborders. Geol Soc Am Spec Pap 55:1-136.
58.
O'Shea TJ, Reep RL (1990): Encephalization quotients and life-history traits in the Sirenia. J Mammal 71:534-543.
59.
Owerkowicz T, Musinsky C, Middleton CM, Crompton AW (2015): Respiratory turbinates and the evolution of endothermy in mammals and birds; in Brainerd EL, Dial K, and Shubin NH (eds): The Great Transformations in Vertebrate Evolution. Chicago, University of Chicago Press, pp 143-465.
60.
Paganin D, Mayo S, Gureyev TE, Miller PR, Wilkins SW (2002): Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc 206:33-40.
61.
Quay WB (1979): The parietal eye-pineal complex; in Glans C, Northcutt RG, Ulinski P (eds): Biology of the Reptilia. New York, Academic Press, 245-406.
62.
Quiroga JC (1980): The brain of the mammal-like reptile Probainognathus jenseni (Therapsida, Cynodontia): a correlative paleo-neoneurological approach to the neocortex at the reptile-mammal transition. J Hirnforsch 21:299-336.
63.
Quiroga JC (1984): The endocranial cast of the advanced mammal-like reptile Therioherpeton cargnini (Therapsida-Cynodontia) from the Middle Triassic of Brazil. J Hirnforsch 25:285-290.
64.
Rey K, Amiot R, Fourel F, Abdala F, Fluteau F, Jalil NE, Liu J, Rubidge BS, Smith RMH, Steyer JS, Viglietti PA, Wang X, Lécuyer C (2017): Oxygen isotopes suggest elevated thermometabolism within multiple Permo-Triassic therapsid clades. eLife 6:e28589.
65.
Rodrigues PG, Ruf I, Schultz CL (2014): Study of a digital cranial endocast of the non-mammaliaform cynodont Brasilitherium riograndensis (Later Triassic, Brazil) and its relevance to the evolution of the mammalian brain. Palaeontol Z 88:329-352.
66.
Roth G, Nishikawa KC, Wake DB (1997): Genome size, secondary simplification, and the evolution of the brain in salamanders. Brain Behav Evol 50:50-59.
67.
Roth JJ, Roth EC, Hotton NN (1986): The parietal foramen and eye: their function and fate in therapsids; in Hotton N, MacLean PD, Roth JJ, Roth ED (eds): Ecology and Biology of Mammal-Like Reptiles. Washington, Smithsonian Institution Press, pp 173-184.
68.
Rowe TB, Macrini TE, Luo Z-X (2011): Fossil evidence on origin of the mammalian brain. Science 332:955-957.
69.
Rubidge BS, Sidor CA (2001): Evolutionary patterns among Permo-Triassic therapsids. Ann Rev Ecol Syst 32:449-480.
70.
Ruf I, Maier W, Rodrigues PG, Schultz CL (2014): Nasal anatomy of the non-mammaliaform cynodont Brasilitherium riograndensis (Eucynodontia, Therapsida) reveals new insight into mammalian evolution. Anat Rec 297:2018-2030.
71.
Ruta M, Botha-Brink J, Mitchell SA, Benton MJ (2014): The radiation of cynodonts and the ground plan of mammalian morphological diversity. Proc Biol Sci 280:20131865.
72.
Safi K, Seid MA, Dechmann DK (2005): Bigger is not always better: when brains get smaller. Biol Lett 22:283-286.
73.
Seymour RS, Bennett-Stamper CL, Johnston SD, Carrier DR, Grigg GC (2004): Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiol Biochem Zool 77:1051-1067.
74.
Shelton CD, Sanders PM (2017): Long bone histology of Ophiacodon reveals the geologically earliest occurrence of fibrolamellar bone in the mammalian stem lineage. Comptes Rendus Palevol 16:397-424.
75.
Sidor CA, Smith RMH (2007): A second burnetiamorph therapsid from the Permian Teekloof Formation of South Africa and its associated fauna. J Vert Paleontol 27:420-430.
76.
Sigogneau D (1970) Revision systematique des gorgonopsiens Sud-Africains. Paris, Cahiers de Paleontologie.
77.
Sigurdsen T, Huttenlocker AK, Modesto SP, Rowe TB, Damiani R (2012): Reassessment of the morphology and paleobiology of the therocephalian Tetracynodon darti (Therapsida), and the phylogenetic relationships of Baurioidea. J Vert Paleontol 32:1113-1134.
78.
Smith RMH (1987): Helical burrow casts of therapsid origin from the Beaufort Group (Permian) of South Africa. Palaeogeogr Palaeoclimatol Palaeoecol 60:155-170.
79.
Tattersall GJ, Leite CAC, Sanders CE, Cadena V, Andrade DV, Abe AS, Milsom WK (2016): Seasonal reproductive endothermy in tegu lizards. Sci Adv 2:e1500951.
80.
Viglietti PA, Smith RMH, Crompton JS (2013): Origin and palaeoenvironmental significance of Lystrosaurus bonebeds in the earliest Triassic Karoo Basin, South Africa. Palaeogeogr Palaeoclimatol Palaeoecol 392:9-21.
© 2017 S. Karger AG, Basel
2017
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.