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 

Introduction

The rich fossil record of amniotes (extant reptiles, birds, mammals, and their extinct relatives) extends over the last 315 million years and spans three eras (Reisz 1997). Whereas Mesozoic dinosaurs and Cenozoic mammals often show evidence of pathology (Lucas and Schoch 1987; Rothschild 1997; Tanke and Rothschild 2002; Witzmann et al. 2008), including bite marks, healed scars, infections, and tumors, they are poorly documented in Paleozoic amniotes (Reisz 1980; Johnson 1988; Reisz and Tsuji 2006; Huttenlocker et al. 2010), the first vertebrates to diversify extensively on land. The pathology reported here was discovered in the anterior part of the lower jaw (Fig. 1) in the largest and presumably oldest known individual of Labidosaurus hamatus, a member of the late Paleozoic group Captorhinidae (Modesto et al. 2007). Captorhinids were the first reptiles to diversify rapidly and disperse globally during the Paleozoic (Müller et al. 2007). They range in size from 25 cm in total length in late Carboniferous (Müller and Reisz 2005) and Early Permian (Heaton and Reisz 1980) forms, and achieve total lengths up to 2.5 m in some of the Middle and Late Permian species (Dodick and Modesto 1995; O'Keefe et al. 2005). During the Early Permian, members of this clade were the most commonly occurring reptiles in the fossil record.
Fig. 1

Evidence of dental and mandibular pathology in L. hamatus, a basal reptile from the Lower Permian of Oklahoma. a Skull reconstruction in right lateral view, modified from Ref. 4. Shaded area represents region of the lower jaw shown in b and c. b CMNH 76876, a right hemimandible in lateral, occlusal, and medial views. c Longitudinal CT scans of the mandible shown in b, illustrating the internal changes that occurred in the anterior region of the jaw as a consequence of the infection. Only one (t2) of the three anterior teeth was functional at the time this individual died. Remnants of the first (rt1) and third (rt3) teeth are visible in the CT scan, and were encapsulated into the mandible by dentary bone, probably after they were broken. Tooth sockets at positions 1 (tp1) and 3 (tp3) have been filled with bone. The direction of infection extends posteriorly from the first tooth position to the fourth open tooth position (ots4) and to the lingual and labial abscesses. It is at the level where the pulp cavity of the teeth would have been in the living organism. Scale bar = 10 mm

The more derived captorhinids evolved dental and cranial specializations as part of their adaptation to omnivory and high-fiber herbivory (Reisz and Sues 2000). In particular they modified their dentition by attaching them very strongly to the jaws through ankylosis, and by changing dramatically the pattern of tooth replacement. The normal pattern of tooth replacement seen in most other Paleozoic tetrapods is characterized by teeth that are relatively loosely attached to the jaw bones, and continuous waves of new teeth erupting at specific tooth positions or sockets, with older teeth being partly resorbed and then shed as the new teeth erupt in the same socket (polyphyodonty). This pattern of tooth replacement is also present in extant tetrapods, including amphibians and most squamates (Edmund 1960). Thus, several teeth in any jaw in certain extant and fossil tetrapods can always be seen in the process of being replaced, with two teeth being present in a single tooth position: the crown of a partially resorbed older tooth from an older wave of replacement and another small tooth from the next wave of replacement growing at the base and slightly lingual to the older tooth (polyphyodonty). With continued resorption, the tooth of the previous wave of replacement is eventually shed and the younger tooth grows into full function in that tooth position (Edmund 1960).

However, in the clade that includes captorhinids like Captorhinus, Labidosaurus, and Moradisaurinae (Fig. 2), the change in the pattern of dental development resulted in a dramatic decrease in tooth replacement waves, with older teeth being removed only occasionally, and by erosion, while new teeth did not erupt in the same tooth position as the older teeth. This highly modified pattern can be best seen in Captorhinus aguti, a species that developed multiple tooth rows (Bolt and DeMar 1975). The development of multiple tooth rows occurred by the eruption of a new series of teeth lingual to the older tooth row, with the wave of eruption extending mesially along the jaw. The older tooth row was not replaced, and instead, an additional row was added. Only the oldest tooth from an older series appears to be occasionally replaced, and only when it appears to be in the way of the new wave (de Ricqles and Bolt 1983).
Fig. 2

Phylogeny of Captorhinidae modified from Müller et al. (2006) and Modesto et al. (2007). Previous studies (Bolt and DeMar 1975; de Ricqles and Bolt 1983; Modesto 1996) show that the evolution of reduced cycles of tooth replacement (RTR) evolved in the ancestor of Captorhinus, moradisaurines (Labidosaurikos, Moradisaurus, Rothianiscus), and Labidosaurus. Skull reconstructions of Romeria texana, C. aguti, Labidosaurikos meachami, and L. hamatus from Heaton (1979), this study, Dodick and Modesto (1995), and Modesto et al. (2007)

The overall result is a dramatic reduction in all derived captorhinids in the replacement of old teeth with new ones. This can be seen even in the single-tooth-rowed forms like Labidosaurus and Captorhinus magnus, where there is usually no gap in the tooth row, and rarely is there any evidence of a tooth in the process of being replaced, as seen in the more basal members of the clade (Modesto 1996). The deep implantation and strong attachment (ankylosis) of the teeth into the jaw were clearly advantageous in these derived captorhinids. In addition, the reduction and changes in tooth replacement also allowed for the development of multiple-tooth-rowed forms through the addition of rows of teeth (Reisz and Sues 2000), a design that is ideally suited for increased oral processing in omnivorous and herbivorous animals like C. aguti and moradisaurine captorhinids.

Careful preparation of several exquisitely preserved specimens while completing a thorough, detailed description of the cranial anatomy of the captorhinid reptile L. hamatus (Modesto et al. 2007) revealed a remarkable pathology in one jaw. Since several complete skulls were prepared as part of that analysis, we are confident of our interpretation that the unusual features of this specimen can be clearly attributed to modifications and damages that occurred during the lifetime of the individual, rather than due to postmortem, taphonomic, or preparatory effects. We employed traditional paleontological techniques and modern computerized tomographic scanning imagery to examine dental pathology in the Lower Permian captorhinid L. hamatus.

Methods

The study specimen is CMNH (Carnegie Museum of Natural History, Pittsburgh, Pennsylvania) specimen 76876, an isolated, partial right hemimandible from the Lower Permian “Labidosaurus pocket” locality near Coffee Creek, Baylor County, TX (Modesto et al. 2007). CMNH 76876 was prepared manually using pneumatic airscribe equipment and pin vises. This specimen was then CT scanned using a Philips MX 8000 QuadCT scanner at Thunder Bay Regional Health Sciences Centre, ON, at 800-μm slice thickness, rendering 24 longitudinal, 44 coronal, and 359 transverse slices.

Results

Examination of CMNH 76876 shows that the teeth in the first and third position were clearly damaged but not replaced in the normal reptilian fashion, in which new teeth emerge from the lingual side of each empty socket. Instead, the tooth sockets were plugged with bone, with the result that fragments of the roots became encapsulated (Fig. 1c), an unusual feature that could only occur while the organism was alive. Farther distally, three open tooth sockets were carefully prepared, and they show partly damaged interdental and strongly damaged lingual and labial walls in an otherwise perfectly preserved region of the mandible. Here, again we were able to determine that the damage developed during the lifetime of the organism, but in this case, the trabecular bone exposed in the enlarged tooth sockets and on the damaged areas around them indicates that these were caused by infection. Similarly, the lateral side of the mandible shows bone destruction in the form of a deep groove that runs posteroventrally from the tooth bearing jaw margin at the level of the damaged interdental wall between tooth sockets 5 and 6, and extends deeply below the cortical layers into the trabecular part of the bone. An internal line, which is visible in CT scans (Fig. 1c), is seen extending from tooth position 1 to 4 and represents internal loss of bone through infection directly beneath the tooth row, and demonstrates clearly the direction of infection extending posteriorly from the first tooth position.

Discussion

Our extensive knowledge of the osteology and patterns of dental replacement in captorhinids, developed over several decades of study of these ancient reptiles, allows us to reconstruct the sequence of events that occurred in this individual. First, there was an initial loss of anterior mandibular teeth, possibly from a trauma, followed by a relatively slow, bony encapsulation that covered the open pulp cavity of the damaged tooth, trapping oral bacteria inside the jaw. The surrounding tissues became involved with the inflammatory reaction through the spread of pyogenic organisms, the acute localized periapical abscess slowly transforming into chronic osteomyelitis (White and Pharoah 2000). The inflammatory reaction extended posteriorly to the level of tooth positions 4–7. There, the osteomyelitis produced a radiolucent area, and quite possibly bony sequestra, resulting in a fistula formation, allowing for the drainage of the pus extraorally. As a consequence of the infection, teeth 4–6 (but not the tooth in position 7) were prematurely exfoliated and the bone of the jaw was irreversibly damaged by osteomyelitis. This interpretation is based on comparisons between the patterns that we see in this specimen with those of extant organisms. It is not possible to determine if this infection caused the death of the individual, but it may have been a major contributing factor, because it appears to have been an active pathology at the time of death and, in some extant lizards, oral osteomyelitis poses a serious health threat (Mehler and Bennett 2003). The dental abscess identified here in the Early Permian L. hamatus predates the previous record for dental pathology in a terrestrial vertebrate reported for late Cretaceous hadrosaurid dinosaurs (Moodie 1930) by nearly 200 million years.

This presence of dental pathology in a reptile that has greatly reduced its tooth replacement pattern is particularly interesting. Among Paleozoic terrestrial vertebrates, lifelong cycles of tooth replacement represent the normal, primitive condition (Edmund 1960). This pattern extends to early amniotes, organisms that include the distant ancestors of most higher vertebrates such as extant mammals, birds, and reptiles, as well as dinosaurs, marine and flying reptiles. This ancient, primitive tooth replacement pattern was modified in various groups either by greatly reducing or eliminating replacement cycles (mammals and some reptiles, like the tuatara, respectively) or by disposing of dentition entirely (turtles and most birds). This evolutionary innovation also occurred within Captorhinidae, the oldest known such example in the fossil record of terrestrial vertebrates.

Our knowledge of this group of ancient reptiles, one of the best known clades of early terrestrial vertebrates, allows us to place this innovation within a broader evolutionary context. The generally accepted phylogenetic relationships among Captorhinidae (Fig. 2) indicates that the reduction in tooth replacement cycles occurred within this family. Early basal members of the clade are small insectivorous and carnivorous predators and have the normal patterns of continual tooth replacement (Modesto 1996; Müller et al. 2006, 2007), whereas the more derived omnivorous and herbivorous members (Sues and Reisz 1998) of the clade have modified and reduced the replacement cycles as part of an evolutionary strategy of developing deeply implanted teeth that are strongly ankylosed to the mandibles (Dodick and Modesto 1995; Jalil and Dutuit 1996). The subsequent development of multiple tooth rows appears to have evolved at least twice within this group and independent of each other (Dodick and Modesto 1995). Clearly, the multiple tooth rows in the upper and lower jaws occluding against each other created a system of oral processing that was superior to that employed by other organisms that used single rows of teeth for occlusion and oral processing (Sues and Reisz 1998; Reisz and Sues 2000; Reisz 2008). Interestingly, an independently evolved reduction in cycles of tooth replacement and dental occlusion for oral processing occurred in synapsids, in the line towards mammals (Rybczynski and Reisz 2001). However, the reduction in synapsids appears to be coupled not only with herbivory but also with the evolution of precise dental occlusion in small carnivorous and insectivorous forms, with deeply implanted teeth and deep, multiple roots (Reisz and Sues 2000).

The obvious success of captorhinids, the first reptiles to diversify extensively and expand globally, suggests that the deep implantation and strong attachment (ankylosis) of the teeth into the jaw probably represented a significant evolutionary advantage. The reduction in tooth replacement also allowed for the evolution of multiple tooth rowed forms through the addition of rows of teeth without any replacement (Bolt and DeMar 1975), the first such occurrence in terrestrial vertebrates. However, if dental damage occurred in large, adult individuals, there was no readily available mechanism to replace the tooth, as would be available in the great majority of other Paleozoic amniotes that had continuous replacement cycles. Thus, the opportunity for mandibular infection from prolonged exposure to oral bacteria was much greater in this reptile than in other Paleozoic amniotes.

This allows us to speculate that our own human system of partial diphyodonty, although of obvious advantage because of its precise dental occlusion and extensive oral processing, is more susceptible to infection than that of our distant ancestors that had a continuous cycle of tooth replacement. Finally, the discovery of dental and mandibular infection from bacteria in a 275million-year-old reptile indicates that interactions between terrestrial amniotes and their microbiota has a very extended history, a feature of vertebrate evolution that has begun to attract the attention of the broad scientific and medical community relatively recently (Ley et al. 2006; Dethlefsen et al. 2006, 2007).

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