#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Histological and developmental insights into the herbivorous dentition of tapinocephalid therapsids


Autoři: Megan. R. Whitney aff001;  Christian A. Sidor aff001
Působiště autorů: Department of Biology and Burke Museum, University of Washington, Seattle, Washington, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223860

Souhrn

Tapinocephalids were one of the earliest therapsid clades to evolve herbivory. In acquiring derived tooth-to-tooth occlusion by means of an exaggerated heel and talon crown morphology, members of this family have long been considered herbivorous, yet little work has been done to describe their dentition. Given the early occurrence of this clade and their acquisition of a dentition with several derived features, tapinocephalids serve as an important clade in understanding adaptations to herbivory as well as macroevolutionary patterns of dental trait acquisition. Here we describe the histology of tapinocephalid jaws and incisors to assess adaptations to herbivory. Our results yield new dental characters for tapinocephalids including a peculiar enamel structure and reduced enamel deposition on the occlusal surface. These traits are convergent with other specialized herbivorous dentitions like those found in ornithischian dinosaurs and ungulates. Furthermore, these results demonstrate that while acquiring some specializations, tapinocephalids also retained plesiomorphic traits like alternate, continuous replacement. We interpret these findings as an example of how different combinations of traits can facilitate a derived and specialized dentition and then discuss their implications in the acquisition of a mammal-like dentition.

Klíčová slova:

Dentin – Dentition – Herbivory – Histology – Jaw – Teeth – Therapsida – Alveolar bone


Zdroje

1. Olson EC. Community Evolution and the Origin of Mammals. Ecology. 1966;47(2): 291–302.

2. Hotton N III, Olson EC, Beerbower R. Amniote Origins and the Discovery of Herbivory. In: Sumida S, Martin KLM, editors. Amniote Origins: Completing the Transition to Land. San Diego: Academic Press Inc; 1998. pp. 207–264.

3. Sues H-D, Reisz RR. Origins and early evolution of herbivory in tetrapods. Trends Ecol Evol. 1998;13(4): 141–145. doi: 10.1016/s0169-5347(97)01257-3 21238234

4. Reisz RR, Sues HD. Herbivory in late Paleozoic and Triassic terrestrial vertebrates. In: Sues HD, editor. Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the fossil record. Cambridge: Cambridge University Press; 2000. pp. 9–41

5. Olson EC. Late Permian Terrestrial Vertebrates, U. S. A. and U. S. S. R. Trans Am Philos Soc. 1962;52(2): 1–224.

6. Brocklehurst N, Day MO, Rubidge BS, Fröbisch J. Olson’s Extinction and the latitudinal biodiversity gradient of tetrapods in the Permian. Proc. R. Soc. B. 2017;284: 20170231. doi: 10.1098/rspb.2017.0231 28381616

7. Olroyd SL, Sidor CA. A review of the Guadalupian (middle Permian) global tetrapod fossil record. Earth Sci Rev. 2017;171: 583–597.

8. Maddin HC, Sidor CA, Reisz RR. Cranial anatomy of Ennatosaurus tecton (Synapsida: Caseidae) from the Middle Permian of Russia, and the evolutionary relationships of Caseidae. J Vertebr Paleontol. 2008;28: 160–180.

9. Cisneros JC, Abdala F, Jashashvili T, Bueno ADO, Dentzien-dias P, Cisneros JC. Tiarajudens eccentricus and Anomocephalus africanus, two bizarre anomodonts (Synapsida, Therapsida) with dental occlusion from the Permian of Gondwana. R Soc Open Sci. 2015;2: 1500900.

10. King GM. The early anomodont Venjukovia and the evolution of the anomodont skull. J Zool. 1994;232: 651–673.

11. King GM. Anomodontia. In: Wellnhofer P, editor. Encyclopedia of paleoherpetology, Part 17C. Stuttgart: Gustav Fischer; 1988. pp. 1–174

12. Rybczynski N, Reisz RR. Earliest evidence for efficient oral processing in a terrestrial herbivore. Nature. 2001;411(6838): 684–687. doi: 10.1038/35079567 11395768

13. King GM. The Dicynodonts: a Study in Palaeobiology. New York: Chapman and Hall; 1990.

14. King GM, Cluver MA. The aquatic Lystrosaurus: an alternative lifestyle. Hist Biol. 1992; 4: 323–341.

15. Whitney MR, Tse YT, Sidor CA. Histological evidence of trauma in tusks of southern African dicynodonts. Pal afr. 2019;53: 75–80.

16. Angielczyk KD. Phylogenetic evidence for and implications of a dual origin of propaliny in anomodont therapsids (Synapsida). Paleobiology. 2004;30(2): 268–296.

17. Crompton AW, Hotton N. Functional morphology of the masticatory apparatus of two dicynodonts (Reptilia, Therapsida). Postilla. 1967;109: 1–51.

18. Hopson JA, Barghusen H. An analysis of therapsid relationships. In: Hotton N, MacLean PD, Roth JJ, Roth EC, editors. The Ecology and Biology of the Mammal-like Reptiles. Washington: Smithsonian Institution Press;1986. pp. 83–106.

19. Kammerer CF. Systematics of the Anteosauria (Therapsida: Dinocephalia). J Syst Paleontol. 2011;9(2): 261–304.

20. Rubidge BS, van den Heever JA. Morphology and systematic position of the dinocephalian Stryacocephalus platyrhynchus. Lethaia. 1997;30: 157–168.

21. Sidor CA. Evolutionary trends and relationships within the Synapsida. Ph.D. Dissertation, University of Chicago, Chicago. 2000.

22. Romer AS. Synapsid evolution and dentition. International Colloquium on the Evolution of Lower and Non Specialized Mammals. 1961;1: 9–56.

23. Boonstra LD. The dentition of the titanosuchian dinocephalians. Ann S Afr Mus. 1962; 46: 57–112.

24. Ivachnenko MF. Estemmenosuches and Primitive Theriodonts from the Late Permian. Paleontolog J. 2000;34(2): 189–197.

25. Güven S, Rubidge B, Abdala F. Cranial morphology and taxonomy of South African Tapinocephalidae (Therapsida: Dinocephalia): the case of Avenantia and Riebeeckosaurus. Pal afr. 2013;48: 24–33.

26. Boonstra LD. The skull of Tapinocephalus and its near relatives. Ann S Afr Mus. 1956; 42: 137–169.

27. Lepper J, Raath MA, Rubidge BS. A diverse dinocephalian fauna from Zimbabwe. S Afr J Sci. 2000;96: 403–405.

28. Rubidge BS. A new primitive dinocephalian mammal-like reptile from the Permian of southern Africa. Palaeontology. 1991;34: 547–559.

29. Sidor CA, Angielczyk KD, Smith RMH, Goulding AK, Nesbitt SJ, Peecook BR, Steyer JS, Tolan S. Tapinocephalids (Therapsida: Dinocephalia) from the Permian Madumabisa Mudstone Formation (Lower Karoo, Mid-Zambezi Basin) of southern Zambia. J Vertebr Paleontol. 2014;34(4): 980–986.

30. Simon RV, Sidor CA, Angielczyk KD, Smith RMHS. First Record of a Tapinocepalid (Therapsida: Dinocephalia) from the Ruhuhu Formation (Songea Group) of Southern Tanzania. J Vertebr Paleontol. 2010;30(4): 1289–1293.

31. Gregory WK. The skeleton of Moschops capensis Broom, a dinocephalian reptile from the Permian of South Africa. Bull Am Mus Nat His. 1926; 56: 179–251.

32. Kemp TS. Mammal-like reptiles and the origin of mammals. London: Academic Press; 1982.

33. LeBlanc ARH, Brink KS, Whitney MR, Abdala F, Reisz RR. Dental ontogeny in extinct synapsids reveals a complex evolutionary history of the mammalian tooth attachment system. Proc R Soc B Biol Sci. 2018;285: 20181792.

34. Broom R. On the Structure of the Skull in the Carnivorous Dinocephalian Reptiles. Proc Zool Soc. 1923;44: 661–84.

35. Boos ADS, Kammerer CF, Shultz CL, Paes Neto VD. A tapinocephalid dinocephalian (Synapsida, Therapsida) from the Rio do Rasto Formation (Paraná Basin, Brazil): Taxonomic, ontogenetic and biostratigraphic considerations. J South Am Earth Sci. 2015;63:375–384.

36. Lamm E. Preparation and Sectioning of Specimens. In: Padian K, Lamm E, editors. Bone histology of fossil tetrapods: advancing methods, analysis, and interpretation. Berkeley, California: University of California Press; 2013. pp. 55–160

37. Erickson GM. Incremental lines of von Ebner in dinosaurs and the assessment of tooth replacement rates using growth line counts. Proc Natl Acad Sci. 1996;93(25): 14623–14627. doi: 10.1073/pnas.93.25.14623 8962103

38. D’Emic MD, Whitlock JA, Smith KM, Fisher DC, Wilson JA. Evolution of High Tooth Replacement Rates in Sauropod Dinosaurs. PLoS One. 2013;8(7): e69235. doi: 10.1371/journal.pone.0069235 23874921

39. Erickson GM. Daily deposition of dentine in Juvenile Alligator and assessment of tooth replacement rates using incremental line counts. J Morphol. 1996;228(2): 189–194. doi: 10.1002/(SICI)1097-4687(199605)228:2<189::AID-JMOR7>3.0.CO;2-0 29852586

40. Fehrenbach MJ, Popowics T. Illustrated Dental Embryology, Histology, and Anatomy: Fourth Edition. Missouri: Elsevier, Inc.; 2016.

41. Dean MC. Comparative observations on the spacing of short-period (von Ebner’s) lines in dentine. Arch Oral Biol. 1998;43(12): 1009–1021. doi: 10.1016/s0003-9969(98)00069-7 9877332

42. Nanci A. Ten Cate’s Oral Histology: Development, Structure, and Function. St. Louis: Mosby Inc. 2008. pp.191–238.

43. O’Meara RN, Dirks W, Martinelli AG. Enamel formation and growth in non-mammalian cynodonts. R Soc Open Sci. 2018;5: 172293. doi: 10.1098/rsos.172293 29892415

44. Sander PM. The microstructure of Reptilian Tooth Enamel: Terminology, Function, and Phylogeny. Münchner Geowissschaftlchen Abhandlugen (A). 1999;38: 1–102.

45. Sander PM. Prismless enamel in amniotes: terminology, functions, and evolution. In: Teaford MF, Smith MM, Ferguson MWJ, editors. Development, Function and Evolution of Teeth. Cambridge: Cambridge University Press; 2000. pp.92–106.

46. Hwang SH. The evolution of dinosaur tooth enamel microstructure. Biol Rev. 2011;86(1): 183–216. doi: 10.1111/j.1469-185X.2010.00142.x 20518758

47. Chen J, LeBlanc ARH, Jin L, Huang T, Reisz RR. Tooth development, histology, and enamel microstructure in Changchunsaurus parvus: Implications for dental evolution in ornithopod dinosaurs. PLoS ONE. 2018;13(11): e0205206. doi: 10.1371/journal.pone.0205206 30403689

48. Jernvall J, Kettunen P, Karavanova I, Martin LB, Thesleff I. Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: Non-dividing cells express growth stimulating Fgf-4 gene. Int J Dev Biol. 1994;38(3): 463–469. 7848830

49. LeBlanc ARH, Reisz RR. Periodontal Ligament, Cementum, and Alveolar Bone in the Oldest Herbivorous Tetrapods, and Their Evolutionary Significance. PLoS One. 2013;8(9): e74697. doi: 10.1371/journal.pone.0074697 24023957

50. Parrington FR. IV—On the tooth-replacement in theriodont reptiles. Phil Trans R Soc Lond B. 1936;226: 212–142.

51. Hopson JA. Tooth replacement in cynodont, dicynodont and therocephalian reptiles. Proc Zool Soc. 1963;142: 625–654.

52. Luo Z, Kielan-jaworowska Z, Cifelli RL. Evolution of dental replacement in mammals. Bull Carnegie Museum of Nat Hist. 2004;9058(36): 159–175.

53. Berkovitz B, Shellis P. The Teeth of Non-Mammalian Vertebrates. London: Academic Press; 2017.

54. Bosshardt DD, Bergomi M, Vaglio G, Wiskott A. Regional structural characteristics of bovine periodontal ligament samples and their suitability for biomechanical tests. J Anat. 2008;212: 319–329. doi: 10.1111/j.1469-7580.2008.00856.x 18304207

55. Beertsen W, McCulloch CAG, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol. 2007;13(1): 20–40.

56. Nishihira N, Yamamoto K, Sato Y, Ishikawa H, Natali AN. Mechanics of periodontal ligament. In: Natali AN, editor. Dental Biomechanics. New York: Taylor and Francis; 2003. pp. 20–34.

57. McCulloch CAG, Lekic P, McKee MD. Role of physical force in regulating the form and function of the periodontal ligament. Periodontology 2000;24: 56–72.

58. Crompton AW, Wood CB, Stern DN. Differential Wear of Enamel: A Mechanism for Maintaining Sharp Cutting Edges. In: Bels L, Chardon M, Vandewalle P, editors. Advances in Comparative and Environmental Physiology, 18. V Berlin, Heidelberg: Springer-Verlag; 1994. pp. 321–346.

59. Fortelius M. Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zoologica Fennica. 1985;180: 1–76.

60. Janis CM. On the means whereby mammals achieve increased functional durability of their dentitions, with special reference to limiting factors. Biol Rev. 1988;63: 197–230. 3042033

61. Sander PM. Non-mammalian synapsid enamel and the origin of mammalian enamel prisms: The bottom-up perspective. In: Wv Koenigswald, Sander PM, editors. Tooth enamel microstructure. Rotterdam: Balkema; 1997. pp. 41–61.

62. Kilic S, Dixon PM, Kempson SA. A light microscopic and ultrastructural examination of calcified dental tissues of horses: 1. The occlusal surface and enamel thickness. Equine Vet J. 1997;29(3): 190–197. doi: 10.1111/j.2042-3306.1997.tb01668.x 9234011

63. LeBlanc ARH, Reisz RR. Patterns of tooth development and replacement in captorhinid reptiles: a comparative approach for understanding the origin of multiple tooth rows. J Vertebr Paleontol. 2015;35: e919928.

64. Boonstra LD. LVII.—On a new tapioncephalid deinocephalian. J Nat Hist Ser 12. 1952;5(53): 509–511.

65. Olejniczak AJ, Grine FE. Assessment of the accuracy of dental enamel thickness measurements using microfocal X-ray computed tomography. Anat Rec—Part A Discov Mol Cell Evol Biol. 2006;288(3): 263–275.

66. Atayman S, Rubidge BS, Abdala F. Taxonomic re-evaluation of tapinocephalid dinocephalians. Pal af. 2009;44: 87–90.

67. Wood CB, Dumont ER, Crompton AW. New Studies of Enamel Micostructure in Mesozoic Mammals: A Review of Enamel Prisms as a Mammalian Synapomorphy. J Mamm Evol. 1999;6(2): 177–213.

68. Grine FE. Prismatic enamel: a pre-adaptation for mammalian diphyodonty? S Afr J Sci. 1980;76(3): 139–141.


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#