Osteomyelitis in a Paleozoic reptile: ancient evidence for bacterial infection and its evolutionary significance
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.
KeywordsPaleozoic tetrapods Osteomyelitis Captorhinidae Dental abscess Early Permian
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).
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.
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.
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.
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).
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).
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