Naturwissenschaften

, 98:551 | Cite as

Osteomyelitis in a Paleozoic reptile: ancient evidence for bacterial infection and its evolutionary significance

  • Robert R. Reisz
  • Diane M. Scott
  • Bruce R. Pynn
  • Sean P. Modesto
Short Communication

Abstract

We report on dental and mandibular pathology in Labidosaurus hamatus, a 275 million-year-old terrestrial reptile from North America and associate it with bacterial infection in an organism that is characterized by reduced tooth replacement. Analysis of the surface and internal mandibular structure using mechanical and CT-scanning techniques permits the reconstruction of events that led to the pathology and the possible death of the individual. The infection probably occurred as a result of prolonged exposure of the dental pulp cavity to oral bacteria, and this exposure was caused by injury to the tooth in an animal that is characterized by reduced tooth replacement cycles. In these early reptiles, the reduction in tooth replacement is an evolutionary innovation associated with strong implantation and increased oral processing. The dental abscess observed in L. hamatus, the oldest known infection in a terrestrial vertebrate, provides clear evidence of the ancient association between terrestrial vertebrates and their oral bacteria.

Keywords

Paleozoic tetrapods Osteomyelitis Captorhinidae Dental abscess Early Permian 

Notes

Acknowledgments

We thank Craig Willson and Janet Loucks, Thunder Bay Regional Health Sciences Centre, for the CT scans; David Berman, CMNH, for the loan of CMNH 76876; and Matt Vickaryous, University of Guelph, for help with the literature search. This research was supported by Discovery Grants from the Natural Sciences and Engineering Research Council of Canada (to RRR and SPM).

References

  1. Bolt JR, DeMar R (1975) An explanatory model of the evolution of multiple rows of teeth in Captorhinus aguti. J Paleontol 49:814–832Google Scholar
  2. de Ricqles A, Bolt JR (1983) Jaw growth and tooth replacement in Captorhinus aguti (Reptilia: Captorhinomorpha): a morphological and histological analysis. J Vertebr Paleontol 3:7–24CrossRefGoogle Scholar
  3. Dethlefsen L, Eckberg PB, Bik EM, Relman DA (2006) Assembly of the human intestinal microbiota. Trends Ecol Evol 21:517–523PubMedCrossRefGoogle Scholar
  4. Dethlefsen L, McFall-Ngai M, Relman DA (2007) An ecological and evolutionary perspective on human–microbe mutualism and disease. Nature 449:811–818PubMedCrossRefGoogle Scholar
  5. Dodick JT, Modesto SP (1995) The cranial anatomy of the captorhinid reptile Labidosaurikos meachami from the Lower Permian of Oklahoma. Palaeontology 38:687–711Google Scholar
  6. Edmund AG (1960) Tooth replacement phenomena in the lower vertebrates. Roy Ont Mus Life Sci Div Contrib 52:1–190Google Scholar
  7. Heaton MJ (1979) Cranial anatomy of primitive captorhinid reptiles from the Late Pennsylvanian and Early Permian, Oklahoma and Texas. Bull Oklahoma Geol Surv 127:1–84Google Scholar
  8. Heaton MJ, Reisz RR (1980) A skeletal reconstruction of the Early Permian captorhinid reptile Eocaptorhinus laticeps (Williston). J Paleontol 54:136–143Google Scholar
  9. Huttenlocker AK, Rega E, Sumida SS (2010) Comparative anatomy and osteohistology of hyperelongate neural spines in the sphenacodontids Sphenacodon and Dimetrodon (Amniota: Synapsida). J Morphol 271:1407–1421PubMedCrossRefGoogle Scholar
  10. Jalil NE, Dutuit JM (1996) Permian captorhinid reptiles from the Argana Formation, Morocco. Palaeontology 39:907–918Google Scholar
  11. Johnson GD (1988) An abnormal captorhinomorph vertebra from the Lower Permian on North-Central Texas. J Vert Paleontol 8(3, Suppl):19AGoogle Scholar
  12. Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848PubMedCrossRefGoogle Scholar
  13. Lucas SG, Schoch RR (1987) Paleopathology of early Cenozoic Coryphodon (Mammalia; Pantodonta). J Vertebr Paleontol 7:145–154CrossRefGoogle Scholar
  14. Mehler SJ, Bennett RA (2003) Oral, dental, and beak disorders of reptiles. Vet Clin North Am Exot Anim Pract 6:477–503PubMedCrossRefGoogle Scholar
  15. Modesto SP (1996) A basal captorhinid reptile from the Fort Sill fissures, Lower Permian of Oklahoma. Oklahoma Geol Notes 56:4–14Google Scholar
  16. Modesto SP, Scott DM, Berman DS, Muller J, Reisz RR (2007) The skull and the palaeoecological significance of Labidosaurus hamatus, a captorhinid reptile from the Lower Permian of Texas. Zool J Linn Soc 149:237–262CrossRefGoogle Scholar
  17. Moodie RL (1930) Dental abscesses in a dinosaur millions of years old, and the oldest yet known. Pac Dent Gaz 38:435–440Google Scholar
  18. Müller J, Reisz R (2005) An early captorhinid reptile (Amniota, Eureptilia) from the Upper Carboniferous of Hamilton, Kansas. J Vertebr Paleontol 25:561–568CrossRefGoogle Scholar
  19. Müller J, Berman DS, Henrici AC, Martens T, Sumida SS (2006) The basal reptile Thuringothryis mahlendorffae (Amniota: Eureptilia) from the Lower Permian of Germany. J Paleontol 80:726–739CrossRefGoogle Scholar
  20. Müller J, Reisz R, Chatterjee S, Kutty S (2007) A passage to India: a small captorhinid from the Upper Permian Kundaram Formation and the postglacial dispersal of early reptiles. J Vertebr Paleontol 27(3, Suppl):121AGoogle Scholar
  21. O'Keefe FR, Sidor CA, Larsson HCE, Maga A, Ide O (2005) The vertebrate fauna of the Upper Permian of Niger—III, morphology and ontogeny of the hindlimb of Moradisaurus grandis (Reptilia, Captorhinidae). J Vertebr Paleontol 25:309–319CrossRefGoogle Scholar
  22. Reisz RR (1980) A protorothyridid captorhinomorph reptile from the Lower Permian of Oklahoma. Life Sci Contrib R Ont Mus 121:1–16Google Scholar
  23. Reisz RR (1997) The origin and early evolutionary history of amniotes. Trends Ecol Evol 12:218–222PubMedCrossRefGoogle Scholar
  24. Reisz RR (2008) Origin of dental occlusion in tetrapods: signal for terrestial vertebrate evolution? J Exp Zool 306B:261–277CrossRefGoogle Scholar
  25. Reisz RR, Sues H-D (2000) Herbivory in late Paleozoic and Triassic terrestrial vertebrates. In: Sues H-D (ed) Evolution of herbivory in terrestrial vertebrates. Cambridge University Press, Cambridge, pp 9–41CrossRefGoogle Scholar
  26. Reisz RR, Tsuji LA (2006) An articulated skeleton of Varanops with bite marks: the oldest known evidence of scavenging among terrestrial vertebrates. J Vertebr Paleontol 26:1021–1023CrossRefGoogle Scholar
  27. Rothschild BM (1997) Dinosauran paleopathology. In: Farlow JO, Brett-Surman MK (eds) The complete dinosaur. Indiana University Press, Indianapolis, pp 427–448Google Scholar
  28. Rybczynski N, Reisz RR (2001) Earliest evidence for efficient oral processing in a terrestrial herbivore. Nature 411:684–687PubMedCrossRefGoogle Scholar
  29. Sues H-D, Reisz RR (1998) Origins and early evolution of herbivory in tetrapods. Trends Ecol Evol 13:141–145PubMedCrossRefGoogle Scholar
  30. Tanke DH, Rothschild BM (2002) Dinosores: an annotated bibliography of dinosaur paleopathology and related topics. Bull New Mex Mus Nat Hist Sci 20:1838–2001Google Scholar
  31. White SC, Pharoah MJ (2000) Oral radiology, principles and interpretation. Mosby Elsevier, St. LouisGoogle Scholar
  32. Witzmann F, Asbach P, Remes K, Hampe O, Hilger A, Paulke A (2008) Vertebral pathology in an ornithopod dinosaur: a hemivertebra in Dysalotosaurus lettowvorbecki from the Jurassic of Tanzania. Anat Rec 291:1149–1155CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Robert R. Reisz
    • 1
  • Diane M. Scott
    • 1
  • Bruce R. Pynn
    • 2
  • Sean P. Modesto
    • 3
  1. 1.Department of BiologyUniversity of Toronto MississaugaMississaugaCanada
  2. 2.Oral and Maxillofacial SurgeryThunder Bay Regional Health Sciences CentreThunder BayCanada
  3. 3.Department of BiologyCape Breton UniversitySydneyCanada

Personalised recommendations