Review of Pathologies on MOR 693: An Allosaurus from the Late Jurassic of Wyoming and Implications for Understanding Allosaur Immune Systems

Jack Thomas Rhodes Wilkin 1 1 Camborne School of Mines, University of Exeter, Penryn, TR10 9FE, United Kingdom.

Keywords: Paleopathology, Dinosauria, Theropoda, Allosaurus, MOR 693.

Abstract

Palaeopathology is important as it provides remarkable insights into the lifestyles of dinosaurs and other prehistoric animals. The Late Jurassic Allosaurus known as Big Al (MOR 693) from Big Horn County, Wyoming preserves at least 19 injuries. About 2% of all showed abnormalities, including on the right foot, on the first phalanx of the third toe, which may have contributed to the animal's death. There would likely have been many more pathologies that did not make it into the paleontological record due do the lack of soft-tissue preservation. Analysis of MOR 693’s immune response to infections and comparing it to other theropods, we can confidently say that dinosaurs possessed an immune system that isolated and localized infections like extant Aves.

Institution Abbreviations MOR, Museum of the Rockies; UUVP, University of Utah Vertebrate Paleontology 1. Introduction

Dinosaur fossils often display evidence of injuries that can be attributed to accidents, old age, predation attempts, intraspecific combat, or metabolic disorders (e.g. Carpenter, 2000; Currie, 2000; Wolff et al., 2009; Rothschild and Depalma, 2013; Foth et al., 2015; Gonzalez et al., 2017;). The specimen being reviewed is a 150 million-year-old Allosaurus fragilis, MOR 693, from the Upper Jurassic Morrison Formation of Big Horn County, Wyoming. The fossil, nicknamed Big Al, is one of the most complete large theropods recovered to date, with 95% of a partially articulated skeleton recovered (Laws, 1996; Hanna, 2002; Bates et al., 2009). Due to the specimen’s completeness, much is known about the animal’s life and death. Arguably the most important, and scientifically compelling, aspect of MOR 693 is the pathologies. MOR 693 had at least 19 injuries that are visible on the skeleton (Laws, 1996; Hanna, 2002; Figure 1; Table 1). Differential diagnosis is possible, especially when, and this is undoubtedly true for MOR 693, most of the skeleton is present.

Figure 1: Skeleton of MOR 693 showing locations of the 19 pathologies. Photograph courtesy of Laura Vietta. Table 1: Descriptions of pathological bones from MOR 693. Adapted from Hanna (2002).

Skeletal abnormalities have three origins 1) trauma-induced, 2) infectious, 3) developmental. Trauma induced pathologies are characterized by boney growths with a rugose texture called a callus (Mann and Murphy, 1990; Marsell and Einhorn, 2012). Infectious pathologies are indicated by an , growths that appear on the surface of the bone (Meyerding, 1927). Penetrating lesions, cloaca, for pus drainage may be present. In an advanced stage of infection, an exostosis, termed involucrum, surrounds the original bone (Ortner and Putschar, 1981). Developmental disorders occur during bone growth and may be caused by genetic defects (Kornak and Mundlos, 2003). MOR 693 has pathologies of all three origins, making it a useful case study.

2. Systematic Description of Pathologies

2.1. Right manual phalanx II-I. The right manual phalanx II-I displays evidence of a healed fracture that was surrounded by substantial bone growth (Figure 2). Thin section examination of the bone under a scanning electron microscope revealed an oblique longitudinal healed fracture line through the bone. Rugose bone growth surrounds the pathology (Laws, 1996; Hanna, 2002). The fracture was likely caused by twisting of the digit.

Figure 2: Manual phalanx II, shown by marker, showing exostosis. Photograph courtesy of Laura Vietti.

The texture and extent of the rugose suggest it was an infection-induced pathology: osteomyelitis (Gross et al., 1993). Small lesions on the growth may be cloaca allowing for pus drainage (Hanna, 2002), a feature consistent with chronic osteomyelitis. Osteomyelitis is the progressive infection of bone and bone marrow by micro-organisms, resulting in inflammatory destruction of bone, bone necrosis and new bone formation (Ikpeme et al., 2010) However, other chronic infectious diseases, for example tuberculosis (Mannepalli et al., 2010) can yield similar traces to osteomyelitis making unequivocal diagnosis difficult. The features that argue against this differential diagnosis are: (1) the sheer amount of bone regeneration, and (2) amount of and diaphyseal involvement (Ortner and Putschar, 1981; Rothschild and Martin, 1993; Aufderheide and Rodriguez-Martin, 1998). Chronic superlative osteomyelitis diagnosis seems the more likely of the two (Hanna, 2002). The cause of the osteomyelitis is also contentious. Osteomyelitis originates from either trauma-induced (Roesgen et al., 1989; Mann and Murphy, 1990) or as a blood-born infection (Mann and Murphy, 1990). If trauma-induced, then the longitudinal fracture must have been open to the elements allowing microbes to enter (Birt et al., 2017) and if blood-borne the infection would have arisen within the intramedullary space (Calhoun et al., 2009). It appears that the fracture preceded osteomyelitis as bone healing is observed and the fracture line is confined to the original bone and does not extend into the exostosis (Hanna, 2002). The above point that of bone healing is important as it suggests that some time had passed from fracture to infection because , bone death caused by the lack of blood supply, occurs in osteomyelitis which inhibits new bone formation (Fondi and Franchi, 2007). Thus, the manus phalanx II-I can be best described as a post-traumatic, hematogenous chronic superlative osteomyelitis (Hanna, 2002).

2.2. Second caudal vertebra.

The chevron of the second caudal vertebra was extensively remodeled following a trauma- induced transverse fracture on the left diaphysis. Exostosis is present on the second caudal vertebra and third dorsal vertebra. However, when dealing with bone abnormalities, one does not presume that the bone remodeling followed an injury, as the third left dorsal rib shows no sign of trauma (Hanna, 2002).

2.3. Dorsal ribs

The third and fifth right dorsal ribs have a rugose callus and the fourth dorsal rib has a smooth callus on the medial shaft. The third, fourth and fifth right dorsal ribs have traumatic healed, misaligned fractures with callus formation which resulted from a violent impact from the right side (Hanna, 2002). The exact cause of this impact is unknown. The third rib also shows evidence of misalignment during healing. The fifth rib shows a putative cloaca for pus drainage due to suppurative osteomyelitis, inflammation of the bone and marrow caused by bacterial infection (Figure 3). Traumatic, healed fractures in the form of calluses are also present on other Allosaurus ribs in the Cleveland-Lloyd Dinosaur Quarry collection (UUVP 2753; UUVP 4946; UUVP 5660; UUVP5661; Hanna, 2002). The bone infection may have been formed as a result of complications during healing (Rega, 2012). `

Figure 3: Pathological right dorsal ribs. Pathologies indicated by triangles. Fifth dorsal rib (left), fourth dorsal rib (center), and third dorsal rib with lesions (insert). Photograph courtesy of Laura Vietti.

The sixth dorsal rib does not appear to have any fractures (Laws, 1996). Although it has a 6.5 cm long spicule on the lateral side. Additionally, the fourteenth right dorsal rib has two bone spicules. The origins for these pathologies are unclear. The spicule on the sixth rib may be a developmental defect due to lack of evidence of bone regrowth or fractures. The spicule on the fourteenth rib may be either traumatic, developmental or isopathic (Hanna, 2002).

2.4. Lateral blade, right scapular.

There is a depression on the lateral blade of the right scapula. Similar pathologies speculated to have been subperiosteal abscesses formed during osteomyelitis with periosteal stripping (Ikpeme et al., 2010) are observed in UUVP 1528 and UUVP 5599. However, in MOR 693, the origin of the pathology is speculative as the depression in the bone would have resulted from early-stage infection that would have begun only a few days before death (Laws, 1996). Instead other possibilities include traumatic tendon avulsion, an unidentified disease process (idiopathic; Hanna, 2002), or aberrancy (Laws, 1996).

2.5. Right pes phalanx III-I.

The most devastating injury which was a contributing factor to the individual's death was a bone infection, osteomyelitis, on the right pes phalanx III-I. Much of the shaft is surrounded by a large exostosis with lesions for pus drainage (Figure 4; Hanna, 2002). The exostosis and lesions are infection-induced caused possibly by a joint infection as these are good locations for microbial entrance. The infection-induced lesions resulted in osteomyelitis and later developed into an involucrum (Laws, 1996). The involucrum resulted from the stripping of the periosteum by the accumulation of pus within the bone, and new bone growing from the periosteum (Moser and Gilbert, 2014). Thus, this pathology can be best described as pyogenic osteomyelitis. The infection itself was long-lived with the infected phalanx rubbing against the other two toes causing significant discomfort (Hanna, 2002).

2.6. Dorsal neural spines.

The dorsal neural spines of MOR 693 shows irregular-shaped exostoses which Hanna (2002) diagnosed as an idiopathic pathological ossification of interspinous ligaments. However, such a feature may not be pathological as ossified tendons are known from other dinosaurs to stiffen the axial skeleton (Organ, 2006), and such structures are not interpreted as pathologic (Foth et al., 2015).

2.7. Left iliac blade.

A thickened area of bone occurs on the dorsal-most margin of the left iliac blade. The region, dorsal of the ischiac peduncle, has a medial-lateral thickness of 4.1 cm, compared to 2.1 on the right iliac blade, and extends for 10 cm along the length of the bone. The origin of the pathology is idiopathic. The thickening may have been trauma-induced. If this were the case, the ilium would have received an avulsion fracture. However, an avulsion fracture would have affected a larger area and would not have been as localized (Hanna, 2002) Figure 4: Involucrum on right pes phalanx III-I. Image courtesy of Laura Vietti.

3. Implications for Allosaur Immune Response

The infections in MOR 693 reveals information about the allosaur immune system. Infections observed in right pes phalanx III-1, metatarsal V, and manus phalanx I-1 of MOR 693, and two pes phalanges III-1 (UUVP 1657 and 6768), pes phalanx IV-1 (UUVP 1851), metatarsal IV (UUVP 30-783), and two scapulae (UUVP 1528 and 5599) are all localized and some are even chronic demonstrating Allosaurus processed an immune response that localized infections preventing them from spreading allowing the animal to live with microbial infection in their bones for prolonged periods (Hanna, 2002).

It is possible that the high number of infected foot bones from allosaurs resulted from allosaurs standing on rotten carcasses which, presumably, would have been teeming with bacteria (Laws, 1996). The ability for theropods to localize chronic infections is also observed in tyrannosaurs suffering from trichomoniasis and suggests an immune response like modern birds. Symptoms of trichomoniasis include swelling and holes in the back of the lower jaw. The disease is prevented from infecting the entire interior of the bone by an innate immune response that localized infections because of the actions of unique avian white blood cells called heterophils (Wolff et al., 2009).

Heterophils are the primary polymorphonuclear leukocytes in birds and are the avian equivalent to mammalian neutrophils (Scanes, 2015). The heterophilic inflammatory response in Aves more closely resembles the reptilian response than the mammalian response to infections (Montaili, 1988).

4. Conclusion

Although none of the pathologies are directly responsible for the death of MOR 693, they did reduce the animal’s ability to obtain food. The infection on pes phalanx III-1 would have rubbed against the adjacent toes causing considerable discomfort.

Sedimentological evidence suggests that the allosaur died in a dried-up riverbed, perhaps driven there by desperation. There is little evidence of vertebrate scavenging on MOR 693. However, the bones do show evidence of beetle burrows, suggesting that the carcass was the dining spot of hundreds to thousands of dermestid beetle larvae (Breithaupt, 2001). Both adult and juvenile dermestids thrive on dried soft tissues, consistent with the paleoenvironmental interpretation of the final resting place being a dried-up riverbed. The pits on the bones are marks left by pupal chambers excavated by the beetles who used the bones as a substrate. Roughly 12% of the skeleton was damaged by beetle activity (Poiner and Poinar, 2008). The beetle damage was caused after post-mortem exposure of the body for a few months, but before the bones were covered by a series of flooding events (Rega, 2012).

MOR 693 provides paleontologists with a remarkable insight into the lifestyles of large theropods. Thanks not only to the completeness of the specimen but also the pathologies, it is possible to reconstruct critical moments in the animal’s life. The ability to localize chronic infections shows an avian-style immune system. Acknowledgements. The author would like to thank Laura Vietta (University of Wyoming) for providing the photographs back in 2015.

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