The Evolution of the Maxillary Canal in Probainognathia (Cynodontia, Synapsida): Reassessment of the Homology of the Infraorbital Foramen in Mammalian Ancestors

Abstract

In mammals, the infraorbital canal provides a passage for the infraorbital ramus of the maxillary branch of the trigeminal nerve. The infraorbital nerve ensures tactile sensitivity of the upper teeth and face between the eye and upper lip and, more significantly, the innervation of mystacial vibrissae (whiskers). In contrast, most non-mammalian synapsids display a more “reptilian-like” ancestral condition in which a long and ramified maxillary canal completely enclosed the infraorbital nerve along with other branches of the trigeminal nerve. The phylogenetic transition from the ancestral “reptilian-like” to the derived “mammal-like” condition has been hypothesized to occur at the base of the Probainognathia clade. Using μCT and synchrotron scanning, this study aims to document this transition in detail by focusing on a sample of non-mammalian probainognathian cynodonts and early mammaliaforms. We find that the mammalian condition is the result of a gradual shortening of the maxillary canal, which enabled the infraorbital nerve to ramify within the soft tissues of the face. Mobile whiskers became possible only after the mammalian infraorbital nerve had evolved, which suggest that these structures appeared in Probainognathus and more derived cynodonts. Finally a foramen located on the ventral margin of the lacrimal bone, which has been often homologized with the infraorbital foramen of derived Probainognathia and early Mammaliaformes, is most probably homologous to the mammalian zygomaticofacial foramen.

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References

  1. Abdala F (2007) Redescription of Platycraniellus elegans (Therapsida, Cynodontia) from the Lower Triassic of South Africa, and the cladistic relationships of eutheriodonts. Palaeontology 50(3):591–618

    Google Scholar 

  2. Abdel-Kader TG, Ali RS, Ibrahim NM (2011) The cranial nerves of Mabuya quinquetaeniata, III: Nervus trigeminus. Life Sci J 8:650–669

    Google Scholar 

  3. Andres KH, von During M, Iggo A, Proske U (1991) The anatomy and fine structure of the echidna Tachyglossus aculeatus snout with respect to its different trigeminal sensory receptors including the electroreceptors. Anat Embryol 184:371–393

    CAS  PubMed  Google Scholar 

  4. 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

  5. Asahara M, Koizumi M, Macrini TE, Hand SJ, Archer M (2016) Comparative cranial morphology in living and extinct platypuses: feeding behavior, electroreception, and loss of teeth. Sci Adv 2 (10):e1601329

    PubMed  PubMed Central  Google Scholar 

  6. Barker CT, Naish D, Newham E, Katsamenis OL, Dyke G (2017) Complex neuroanatomy in the rostrum of the Isle of Wight theropod Neovenator salerii. Sci Rep 7:3749

    PubMed  PubMed Central  Google Scholar 

  7. Barone R (1999) Anatomie comparée des mammifères domestiques. Tome 1: Ostéologie. 3ème édition. Vigot, Paris

  8. Bellairs AD’A (1949) Observations on the snout of Varanus, and a comparison with that of other lizards and snakes. J Anat 83:116–146

    PubMed  PubMed Central  Google Scholar 

  9. Bendel E-M, Kammerer CF, Kardjilov N, Fernandez V, Fröbisch J (2018) Cranial anatomy of the gorgonopsian Cynariops robustus based on CT-reconstruction. PLoS One 13(11): e0207367

    PubMed  PubMed Central  Google Scholar 

  10. Benoit J, Angielczyk KD, Miyamae JA, Manger PR, Fernandez V, Rubidge BS (2018) Evolution of facial innervation in anomodont synapsids (Synapsida): insights from X-ray computerized microtomography. J Morphol 279 (5): 673–701

    PubMed  Google Scholar 

  11. Benoit J, Fernandez V, Manger PR, Rubidge BS (2016b) Cranial bosses of Choerosaurus dejageri (Synapsida, Therocephalia): earliest evidence of cranial display structures in eutheriodonts. PLoS One 11(8):e0161457

    PubMed  PubMed Central  Google Scholar 

  12. Benoit J, Jasinoski S (2016) Picking up the pieces: the digital reconstruction of a destroyed holotype from its serial section drawings. Palaeontol Electron 19.3.3T: 1–16

    Google Scholar 

  13. Benoit J, Manger PR, Norton LA, Fernandez V, Rubidge BS (2017b) Synchrotron scanning reveals the palaeoneurology of the head-butting Moschops capensis (Synapsida, Dinocephalia). PeerJ 5:e3496

    PubMed  PubMed Central  Google Scholar 

  14. Benoit J, Manger PR, Rubidge BS (2016a) Palaeoneurological clues to the evolution of defining mammalian soft tissue traits. Sci Rep 6:25604. https://doi.org/10.1038/srep25604

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Benoit J, Norton LA, Manger PR, Rubidge BS (2017a) Reappraisal of the envenoming capacity of Euchambersia mirabilis (Synapsida, Therocephalia) using μCT-scanning techniques. PLoS One 12(2): e0172047

    PubMed  PubMed Central  Google Scholar 

  16. Bonaparte JF, Barberena MC (2001) On two advanced carnivorous cynodonts from the Late Triassic of southern Brazil. Bull Mus Comp Zool 156: 59–80

    Google Scholar 

  17. Bonaparte JF, Crompton AW (2017) Origin and relationships of the Ictidosauria to non-mammalian cynodonts and mammals. Hist Biol 30: 174–182. https://doi.org/10.1080/08912963.2017.1329911

    Article  Google Scholar 

  18. Bonaparte JF, Martinelli AG, Schultz CL (2005) New information on Brasilodon and Brasilitherium (Cynodontia, Probainognathia) from the Late Triassic of southern Brazil. Rev Bras Paleontol 8: 25–46

    Google Scholar 

  19. Bonaparte JF, Martinelli AG, Schultz CL, Rubert R (2003) The sister group of mammals: small cynodonts from the Late Triassic of southern Brazil. Rev Bras Paleontol 5:5–27

    Google Scholar 

  20. Bonnan MF (2016) The Bare Bones: An Unconventional Evolutionary History of the Skeleton. Indiana University Press, Bloomington & Indianapolis

    Google Scholar 

  21. Born G (1879) Die Nasenhöhlen und der Thränennasengang der amnioten Wirbeltiere. Morphol Jb 5: 62–137

    Google Scholar 

  22. Botha-Brink J, Bento Soares M, Martinelli AG (2018) Osteohistology of Late Triassic prozostrodontian cynodonts from Brazil. PeerJ 6:e5029. https://doi.org/10.7717/peerj.5029

    Article  PubMed  PubMed Central  Google Scholar 

  23. Brink AS (1960a) On some small therocephalians. Palaeontol Afr 7: 155–182

    Google Scholar 

  24. Brink AS (1960b) A new type of primitive cynodont. Palaeontol Afr 7:119–154

    Google Scholar 

  25. Brink AS (1986) Illustrated Bibliographical Catalogue of the Synapsida: Part 1. Handbook of the Geological Survey of South Africa. Geological Survey, Pretoria

    Google Scholar 

  26. Brink AS (1987) Illustrated Bibliographical Catalogue of the Synapsida: Part 2. Handbook of the Geological Survey of South Africa. Geological Survey, Pretoria

    Google Scholar 

  27. Carlson KJ, Stout D, Jashashvili T, de Ruiter DJ, Tafforeau P, Carlson K, Berger LR (2011) The endocast of MH1, Australopithecus sediba. Science 333 (6048): 1402–1407

    CAS  PubMed  Google Scholar 

  28. Castanhinha R, Araújo R, Júnior LC, Angielczyk KD, Martins GG, Martins RMS, 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(12) : e80974

    PubMed  PubMed Central  Google Scholar 

  29. Cau A, Beyrand V, Voeten DFAE, Fernandez V, Tafforeau P, Stein K, Barsbold R, Tsogtbaatar K, Currie PJ, Godefroit P (2017) Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs. Nature 552(7685): 395.

    CAS  PubMed  Google Scholar 

  30. Cluver MA (1971) The cranial morphology of the dicynodont genus Lystrosaurus. Ann So Afr Mus 56: 155–274

    Google Scholar 

  31. Crompton AW, Musinsky C, Owerkowicz T (2015) Evolution of the mammalian nose. In: Dial KP, Shubin N, Brainerd EL (eds), Great Transformations in Vertebrate Evolution. University of Chicago Press, Chicago, pp 189–205

  32. Crompton AW, Owerkowicz T, Bhullar B-A, Musinsky C (2017) Structure of the nasal region of non-mammalian cynodonts and mammaliaforms: speculations on the evolution of mammalian endothermy. J Vertebr Paleontol 37: e1269116

    Google Scholar 

  33. Cunningham JA, Rahman IA, Lautenschlager S, Rayfield EJ, Donoghue PDJ (2014) Virtual world of paleontology. Trends Ecol Evol 29: 347–357

    PubMed  Google Scholar 

  34. Dal Sasso C, Maganuco S, Buffetaut E, Mendez MA (2005) New information on the skull of the enigmatic theropod Spinosaurus, with remarks on its size and affinities. J Vertebr Paleontol 25: 888–896

    Google Scholar 

  35. Estes R (1961) Cranial anatomy of the cynodont reptile Thrinaxodon liorhinus. Bull Mus Comp Zool 125: 165–180

    Google Scholar 

  36. Evans HE, Lahunta A de (2012) Miller's Anatomy of the Dog, 4th edition. Elsevier, Saunders, Philadelphia

  37. Fernandez V, Abdala F, Carlson KJ, Cook DC, Rubidge BS, Yates A, Tafforeau P (2013) Synchrotron reveals Early Triassic odd couple: injured amphibian and aestivating synapsid share burrow. PLoS One 8(6):e64978

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Fourie S (1974) The cranial morphology of Thrinaxodon liorhinus Seeley. Ann So Afr Mus 65: 337–400

    Google Scholar 

  39. Gow CE (1986) The side wall of the braincase in cynodont synapsids, and a note on the homology of the mammalian promontorium. So Afr J Zool 21:136–148

    Google Scholar 

  40. Grant RA, Haidarliu S, Kennerley NJ, Prescott TJ (2013) The evolution of active vibrissal sensing in mammals: evidence from vibrissal musculature and function in the marsupial opossum Monodelphis domestica. J Exp Biol 216: 3483–3494

    PubMed  Google Scholar 

  41. Hahn G (1985) Zum Bau des infraorbital-foramens bei den Paulchoffatiidae (Multituberculata, Ober Jura). Berliner geowiss Abh A 60: 5–27

    Google Scholar 

  42. Hoffman EA, Rowe TB (2018) Jurassic stem-mammal perinates and the origin of mammalian reproduction and growth. Nature 561:104–108. https://doi.org/10.1038/s41586-018-0441-3

    CAS  Article  PubMed  Google Scholar 

  43. Hopson JA (1973) Endothermy, small size, and the origin of mammalian reproduction. Am Nat 107 (955): 446–452

    Google Scholar 

  44. Hopson JA (1990) Cladistic analysis of synapsid relationships. J Vertebr Paleont 10 (3 Suppl): 28A

    Google Scholar 

  45. Hopson JA, Kitching JW (2001) A probainognathian cynodont from South Africa and the phylogeny of nonmammalian cynodonts. Bull Mus Comp Zool 156: 5–35

    Google Scholar 

  46. Horovitz I, Martin T, Bloch J, Ladeveze S, Kurz C, Sanchez-Villagra M (2009) Cranial anatomy of the earliest marsupials and the origin of opossums. PLoS One 4(12): e8278.

    PubMed  PubMed Central  Google Scholar 

  47. Hu Y, Meng J, Li C, Wang Y (2010) New basal eutherian mammal from the Early Cretaceous Jehol biota, Liaoning, China. Proc Roy Soc B 277(1679): 229–236. https://doi.org/10.1098/rspb.2009.0203

    Article  Google Scholar 

  48. Huber E (1930) Evolution of facial musculature and cutaneous field of trigeminus. Part I. Q Rev Biol 5(2): 133–188

    Google Scholar 

  49. Ibrahim N, Sereno PC, Dal Sasso C, Maganuco S, Fabbri M, Martill DM, Zouhri S, Myhrvold N, Iurino DA (2014) Semiaquatic adaptations in a giant predatory dinosaur. Science 345(6204):1613–1616

    CAS  PubMed  Google Scholar 

  50. Kemp TS (1969) On the functional morphology of the gorgonopsid skull. Philos Trans R Soc Lond B Biol Sci 256: 1–83

    Google Scholar 

  51. 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

    Google Scholar 

  52. Kemp TS (1983) The relationships of mammals. Zool J Linn Soc 77: 353–384

    Google Scholar 

  53. Kerekes P, Daret A, Shulz DE, Ego-Stengel V (2017) Bilateral discrimination of tactile patterns without whisking in freely running rats. J Neurosci 37(32): 7567–7579

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  55. Krause DW, Wible JR, Hoffmann S, Groenke JR, O’Connor PM, Holloway WL, Rossie JB (2014) Craniofacial morphology of Vintana sertichi (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar. J Vertebr Paleontol 34 supp1: 14–109

    Google Scholar 

  56. Kühne WG (1956) The Liassic Therapsid Oligokyphus. British Museum Natural History, London

    Google Scholar 

  57. Laaß M, Kaestner A (2017) Evidence for convergent evolution of a structure comparable to the mammalian neocortex in a Late Permian synapsid. J Morphol 278: 1033–1057

    PubMed  Google Scholar 

  58. Laaß M Schillinger B (2015) Reconstructing the auditory apparatus of synapsids by means of neutron tomography. Physics Procedia 69: 628–635

    Google Scholar 

  59. Leitch DB, Catania KC (2012) Structure, innervation and response properties of integumentary sensory organs in crocodilians. J Exp Biol 215: 4217–4230

    PubMed  PubMed Central  Google Scholar 

  60. Leo JT, Cassell MD, Bergman RA (1995) Variation in human infraorbital nerve, canal and foramen. Ann Anat 177 : 93–95.

    CAS  PubMed  Google Scholar 

  61. Lillegraven JA, Krusat G (1991) Craniomandibular anatomy of Haldanodon exspectatus (Docodontia; Mammalia) from the Late Jurassic of Portugal and its implications to the evolution of mammalian characters. Contrib Geol Univ Wyoming 28: 39–138

    Google Scholar 

  62. Lingham-Soliar T (2014) The Vertebrate Integument Volume 1. Springer-Verlag, Berlin, Heidelberg

    Google Scholar 

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

    Google Scholar 

  64. Luo Z-X (1994) Sister−group relationships of mammals and transformations of diagnostic mammalian characters. In: Fraser NC, Sues H-D (eds), In the Shadow of the Dinosaurs: Early Mesozoic Tetrapods. Cambridge University Press, Cambridge, pp 98–128

    Google Scholar 

  65. Luo Z-X, Chen PJ, Li G, Chen M (2007) A new eutriconodont mammal and evolutionary development in early mammals. Nature 446: 288–293

    CAS  PubMed  Google Scholar 

  66. Luo Z-X, Crompton AW, Sun AL (2001) A new mammaliaform from the Early Jurassic and evolution of mammalian characteristics. Science 292 (5521): 1535–1540

    CAS  PubMed  Google Scholar 

  67. Lyckegaard A, Johnson G, Tafforeau P (2011) Correction of ring artifacts in X-ray tomographic images. Internatl J Tomogr Stat 18: 1–9

    Google Scholar 

  68. Manger PR, Pettigrew JD (1996) Ultrastructure, number, distribution and innervation of electroreceptors and mechanoreceptors in the bill skin of the platypus. Brain Behav Evol 48: 27–54

    CAS  PubMed  Google Scholar 

  69. Martinelli AG, Bonaparte JF (2011) Postcanine replacement in Brasilodon and Brasilitherium (Cynodontia, Probainognathia) and its bearing in cynodont evolution. In: Calvo J, Porfiri J, González Riga B, Dos Santos D (eds) Dinosaurios y Paleontología desde América Latina, Anales del III Congreso Latinoamericano de Paleontología (Neuquén, 2008). Editorial de la Universidad Nacional de Cuyo, Mendoza, pp 179–186

  70. Martinelli AG, Corfe IJ, Gill PG, Kallonen A, Rayfield EJ, Rodrigues PB, Schultz CL, Soares MB (2017c) Brasilodon quadrangularis, Brasilitherium riograndensis and Minicynodon maieri (Cynodontia): taxonomy, ontogeny and tooth replacement. In: Paleontologia em Destaque, Boletim de Resumos XXV Congresso Brasileiro de Paleontologia, Ribeirão Preto, SP, Brazil, p 189

  71. Martinelli AG, Eltink E, Da-Rosa AAS, Langer MC, Angielczyk K (2017b) A new cynodont from the Santa Maria Formation, south Brazil, improves Late Triassic probainognathian diversity. Pap Palaeontol 3: 401–423

    Google Scholar 

  72. Martinelli AG, Soares MB (2016) Evolution of South American non-mammaliaform cynodonts (Synapsida, 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. Museo Argentino de Ciencias Naturales, Buenos Aires, pp 183–196

  73. Martinelli AG, Soares MB, de Oliveira TV, Rodrigues PG, Schultz CL (2017a) The Triassic eucynodont Candelariodon barberenai revisited and the early diversity of stem prozostrodontians. Acta Palaeontol Pol 62(3): 527–542

  74. Martínez RN, Fernandez E, Alcober OA (2013) A new non-mammaliaform eucynodont from the Carnian-Norian Ischigualasto Formation, northwestern Argentina. Rev Bras Paleontol 16(1): 61–76. https://doi.org/10.4072/rbp.2013.1.05

    Article  Google Scholar 

  75. Martínez RN, Forster CA (1996) The skull of Probelesodon sanjuanensis, sp. nov., from the Late Triassic Ischigualasto Formation of Argentina. J Vertebr Paleontol 16(2): 285–291

    Google Scholar 

  76. Martínez RN, May CL, Forster CA (1996) A new carnivorous cynodont from the Ischigualasto Formation (Late Triassic, Argentina), with comments on eucynodont phylogeny. J Vertebr Paleontol 16(2): 271–284

    Google Scholar 

  77. Martins C, Li X, Rhoton AL Jr (2003) Role of the zygomaticofacial foramen in the orbitozygomatic craniotomy: anatomic report. Neurosurgery. 53(1): 168–172

  78. Mead JG, Fordyce RE (2009) The therian skull: a lexicon with emphasis on the odontocetes. Smithsonian Contrib Zool 627: 1–248

  79. 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 Instrum Methods Phys Res Sect B 324: 41–48

    CAS  Google Scholar 

  80. Mitchinson B, Grant RA, Arkley K, Rankov V, Perkon I, Prescott TJ (2011) Active vibrissal sensing in rodents and marsupials. Philos Trans R Soc B Biol Sci 366: 3037–3048

    Google Scholar 

  81. Miyamae JA, Bhullar BS (2017) Comparative morphology of the trigeminal canal and a scenario for the evolution of facial musculature in mammals. 77th Annual meeting of the Society of Vertebrate Paleontology, August 2017, Calgary, Canada.

  82. Mohamed R (2018) Anatomical and radiographic study on the skull and mandible of the common opossum (Didelphis marsupialis Linnaeus, 1758) in the Caribbean. Vet Sci 5(2): 44. https://doi.org/10.3390/vetsci5020044

    Article  PubMed Central  Google Scholar 

  83. Muchlinski MN (2008) The relationship between the infraorbital foramen, infraorbital nerve, and maxillary mechanoreception: implications for interpreting the paleoecology of fossil mammals based on infraorbital foramen size. Anat Rec 291: 1221–1226

    Google Scholar 

  84. Muchlinski MN (2010) A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals. J Hum Evol 58, 447–473

    PubMed  Google Scholar 

  85. Muchlinski MN, Wible JR, Corfe I, Sullivan M, Grant RA (2018) Good vibrations: the evolution of whisking in small mammals. Anat Rec. https://doi.org/10.1002/ar.23989

  86. 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: 1063–1079

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Novacek MJ (1986) The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bull Am Mus Nat Hist 183: 1–111

    Google Scholar 

  88. Nxumalo MP, Benoit J (2018) The phylogenetic classification and locomotion of a non-mammaliaform cynodont Lumkuia fuzzi (Probainognathia, Cynodontia) based on CT-tomography of the postcranial skeleton. 20th Biennial Conference of the Palaeontological Society of Southern Africa, July 2018, Bloemfontein, South Africa

  89. Oliveira TV, Soares MB, Schultz CL (2010) Trucidocynodon riograndensis gen. nov. et sp. nov. (Eucynodontia), a new cynodont from the Brazilian Upper Triassic (Santa Maria Formation). Zootaxa 2382: 1–71

  90. Pacheco CP, Martinelli AG, Pavanatto AEB, Soares MB, Dias-da-Silva S (2017) Prozostrodon brasiliensis, a probainognathian cynodont from the Late Triassic of Brazil: second record and improvements on its dental anatomy. Hist Biol 30: 475–485. https://doi.org/10.1080/08912963.2017.1292423

    Article  Google Scholar 

  91. Paganin D, Mayo SC, Gureyev TE, Miller PR, Wilkins SW (2002) Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microscop 206(1): 33–40

    CAS  Google Scholar 

  92. Rodella LF, Buffoli B, Labanca M, Rezzani R (2012) A review of the mandibular and maxillary nerve supplies and their clinical relevance. Arch Oral Biol 57(4): 323–334

    CAS  PubMed  Google Scholar 

  93. Rodrigues PG, Martinelli AG, Schultz CL, Corfe IJ, Gill PG, Soares MB, Rayfield EJ (2018) Digital cranial endocast of Riograndia guaibensis (Late Triassic, Brazil) sheds light on the evolution of the brain in non-mammalian cynodonts. Hist Biol. https://doi.org/10.1080/08912963.2018.1427742

  94. 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: 291–307

    Google Scholar 

  95. 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. Paläontol Z 88: 329–352

    Google Scholar 

  96. Romer AS (1969a) The Brazilian Triassic cynodont reptiles Belesodon and Chiniquodon. Breviora 332: 1–16

    Google Scholar 

  97. Romer AS (1969b) The Chañares (Argentina) Triassic reptile fauna V. A new chiniquodontid cynodont, Probelesodon lewisi - cynodont ancestry. Breviora 333: 1–24

    Google Scholar 

  98. Romer AS (1970) The Chañares (Argentina) Triassic reptile fauna. VI. A chiniquodontid cynodont with an incipient squamosal-dentary jaw articulation. Breviora 344: 1–18

    Google Scholar 

  99. Rougier GW, Wible JR, Beck RMD, Apesteguía S (2012) The Miocene mammal Necrolestes demonstrates the survival of a Mesozoic nontherian lineage into the late Cenozoic of South America. Proc Natl Acad Sci USA 109(49): 20053–20058

    CAS  PubMed  Google Scholar 

  100. Rowe T, 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 USA 105(4): 1238–1242

    CAS  PubMed  Google Scholar 

  101. Rowe TB, Shepherd GM (2016) Role of ortho-retronasal olfaction in mammalian cortical evolution. J Comp Neurol 524(3): 471–495

    PubMed  Google Scholar 

  102. Ruf I, Maier W, Rodrigues PG, Schultz CL (2014) Nasal anatomy of the non-mammaliaform cynodont Brasilitherium riograndensis (Eucynodontia, Synapsida) reveals new insight into mammalian evolution. Anat Rec 297: 2018–2030

    Google Scholar 

  103. 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

    Google Scholar 

  104. Santos German IJ, Buchaim DV, Andreo JC, Shinohara EH, Capelozza AL, Shinohara AL, Rosa Junior GM, Pereira M, Buchaim RL (2015) Identification of the bony canal of the posterior superior alveolar nerve and artery in the maxillary sinus: tomographic, radiographic, and macroscopic analyses. Sci World J 2015. https://doi.org/10.1155/2015/878205

  105. Schaller O (1992) Illustrated Veterinary Anatomical Nomenclature. Ferdinand Enke Verlag, Stuttgart

    Google Scholar 

  106. Shoshani J (1986) Mammalian phylogeny: comparison of morphological and molecular results. Mol Biol Evol 3(3): 222–242

    CAS  PubMed  Google Scholar 

  107. Simpson GG (1933) The ear region and the foramina of the cynodont skull. Am J Sci 26: 285–294

    Google Scholar 

  108. Sisson S (1910) A Textbook of Veterinary Anatomy. Saunders Company, Philadelphia and London

    Google Scholar 

  109. Soares MB, Schultz CL, Horn BLD (2011) New information on Riograndia guaibensis Bonaparte, Ferigolo & Ribeiro, 2001 (Eucynodontia, Tritheledontidae) from the Late Triassic of southern Brazil: anatomical and biostratigraphic implications. An Acad Bras Ciênc 83: 329–354

    PubMed  Google Scholar 

  110. Sofroniew NJ, Svoboda K (2015) Whisking. Curr Biol 25, R137–R140

    CAS  PubMed  Google Scholar 

  111. 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: 217–268

    Google Scholar 

  112. Tatarinov LP (1976) Morphological Evolution of the Theriodonts and the General Problems of Phylogenetics. NAUKA, Moscow [in Russian]

    Google Scholar 

  113. Van Valen L (1960) Synapsids as mammals. Evolution 14: 304–313

    Google Scholar 

  114. Watson DMS (1931) On the skeleton of a bauriamorph reptile. J Zool 1931: 1163–1205

    Google Scholar 

  115. Weitkamp T, Haas D, Wegrzynek D, Rack A (2011) ANKAphase: software for single-distance phase retrieval from inline X-ray phase-contrast radiographs. J Synchrotron Radiat 18(4): 617–629

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  117. Wible JR (2008) On the cranial osteology of the Hispaniolan solenodon, Solenodon paradoxus Brandt, 1833 (Mammalia, Lipotyphla, Solenodontidae). Ann Carnegie Mus 77: 321–402

    Google Scholar 

  118. Wible JR (2011) On the treeshrew skull (Mammalia, Placentalia, Scandentia). Ann Carnegie Mus 79(3): 149–230

    Google Scholar 

  119. Witmer LM (1995) Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. J Morphol 225: 269–327

    PubMed  Google Scholar 

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Acknowledgments

The authors thank Cesar Leandro Schultz, Marina Bento Soares, José Fernando Bonaparte, Bhart-Anjan Bhullar, and Timothy Rowe for access to CT data. Specimen UFRGS-PV-1043-T was scanned at Fachhochschule Aalen with the support of the Alexander von Humboldt Foundation. We acknowledge the European Synchrotron Radiation Facility for provision of synchrotron radiation facilities and we would like to thank Paul Tafforeau for assistance in using beamline ID19. We thank John Wible, Ricardo Araújo, and an anonymous reviewer whose comments helped to improve the manuscript. This research was conducted with financial support from the Claude Leon Foundation; PAST and its scatterlings projects; the NRF African Origins Platform; and the DST-NRF Centre of Excellence in Palaeosciences (CoE in Palaeosciences). Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to the CoE in Paleosciences. The authors declare no competing interest.

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Correspondence to Julien Benoit.

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Benoit, J., Ruf, I., Miyamae, J.A. et al. The Evolution of the Maxillary Canal in Probainognathia (Cynodontia, Synapsida): Reassessment of the Homology of the Infraorbital Foramen in Mammalian Ancestors. J Mammal Evol 27, 329–348 (2020). https://doi.org/10.1007/s10914-019-09467-8

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Keywords

  • Mammaliaformes
  • Trigeminal nerve
  • Whiskers
  • Zygomatic nerve
  • Lacrimal canal