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Volume 1 Number 4 Article 38

8-16-1987

Evolutionary Aspects of Reptilian and Mammalian Enamel Structure

A. Sahni Panjab University

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Recommended Citation Sahni, A. (1987) "Evolutionary Aspects of Reptilian and Mammalian Enamel Structure," Scanning Microscopy: Vol. 1 : No. 4 , Article 38. Available at: https://digitalcommons.usu.edu/microscopy/vol1/iss4/38

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EVOLUTIONARYASPECTS Of REPTILIANAND MAMMALIAN ENAMEL STRUCTURE

A Sahni

Centre of Advanced Study in Geology, Panjab University CHANDIGARH-160014India

(Received for publication December 08, 1986, and in revised form August 16, 1987)

Abstract Introduction

The of enamel structure is dealt The present paper focusses attention on the with here on the basis of reptiles and evolution of mammalian enamels based principally ranging from the to the present. on the evidence of fossil vertebrates. This The evidence suggests that prismatic enamel had aspect involves not only the documentation of the developed in some reptiles and the stages leading to the development of prismatic , about 180 million years ago. enamels, but also the study of the structural For the next 100 million years, mammalian diversity of recent reptiles and mammals. While evolutionary history is sparingly documented and the prism packing patterns of extant reptiles and this is reflected in the poor record of enamel mammals has become better understood through the evolution during this period. The few works of Cooper and Poole (1973) and Boyde (1964), reptiles and mammals studied suggest a pre­ there is still a lacuna with regard to the fossil prismatic structure. In the Late (BO record. During the last decade, considerable to 65 million years ago) when the fossil record attention has been paid to the enamel structure of improves, mammalian enamel investigated from North fossil-based evolutionary lineages, particularly American localities, are found to be prismatic; those concerning the Rodentia, Cetacea and allotherian (multituberculate) and metatherian Primates. This has largely become possible () enamels are usually tubular, while because of a multidisciplinary approach involving eutherian (placental) ones are not. Prism palaeontologists and dental histologists, and the structure in Tertiary mammals in general, conforms growing awareness that enamels of fossilized to that of their present day descendants, but mammals have an excellent potential for there are discernible exceptions. The record of documenting structural diversity on a scale much evolutionary change in Tertiary mammals is larger than that known for living mammals. obscured by functional modifications related to Furthermore, all previous studies have shown that biomechanical stresses. Enamel structure may be fossilized mineralized tissue undergoes negligible secondarily modified; similar in phylogenetically diagenetic alteration through time and faithfully unrelated groups (eg., pauciserial enamel of early records the prism structure, even in that ) or dissimilar at the intra-familial level are more than 200 million years old. (eg., families Ctenodactylidae and The pioneering efforts of Poole (1956, 1957) Ischryomyicae). Prismatic enamel is recorded from and Moss (1969) in studying fossil material by the tooth of a hatchling of the gavial, Gavialis light microscopy have recently been taken up gangeticus. world-wide by several workers using scanning electron microscopy (Fosse et al. 1973, 1978, 1985; Carl son and Krause 1985; Koenigswald 1980; Boyde and Martin 1984; Kozawa 1984; Sahni 1979). While this has led to a better documentation of the enamel structure of diverse fossil organism, these studies have mainly been descriptive accounts of prism patterns and have lacked a theoretical model to interpret evolutionary mech­ anisms. There are still several unsolved issues that preclude a better understanding of the evo­ KEHIORDS: Fossil reptile, mammal, Enamel lutionary processes in various recent and fossil evolution, geochronological distribution, prism organisms. Some of these points are discussed patterns and structure. below. Correspondence of phylogenies based on enamel structure and gross dental morphology

Many workers have emphasized the value of

1903 A. Sahni enamel structure in establishing phylogenetic Structure in relation to function relationships (Fosse et al. 1978; Carlson and Krause 1985; Flynn 1982; Koenigswald 1980; Boyde The adaptive response of enamel structure at and Martin 1984). In general, the prism packing the crystallite and prism pattern level to such patterns follow taxonomic relationships estab­ biomechanical stresses generated by crown size, lished by evolutionary biologists. Primate, pro­ hypsodonty, rootless conditions, leading and boscidean, and taenioloabidoid multi­ trailing wear margins, and lophodonty is only now tuberculate enamel are characterized by a pre­ becoming better understood (Koenigswald 1980; dominance of Pattern 3 prisms, but their enamel Fortelius 1984; Rensberger and Koenigswald 1980). ultrastructure is clearly distinguishable even in This aspect is important because functionally small samples. The ungulates (both artiodactyls related changes in the enamel structure may be and perissodactyls) are characterized by Pat tern lost or reintroduced several times in phylogenetic 2 prisms along with the . Amongst all lineages and tend to obscure the main mammalian orders, the rodents represent the most evolutionary trends of a particular lineage. Such unified group on the basis of enamel ultrastruc­ modifications are not only significant at gross ture even though there are sharp and distinct levels, but also at levels of resolution by differences in enamel at the subordinal level. electron microscopy. The great variety of prism arrangements at various With the exception of some hypsodont arvi­ taxonomic levels hinders, in many ways, the colid rodents, in which the teeth are also delineation and record of phylogenetic lineages. rootless, the structure of the incisor is usually Though precise correspondence at lower taxo­ different from that of the molars. This diff­ nomic levels is usually lacking, there is a erentiation can first be observed in the incisors general congruity between evolutionary lineages of the ptilodontid multi tuberculate based on enamel ultrastructure and those based on (Sahni 1979). The structure of the rodent incisor dental or cranial characteristics. This aspect is has been studied in better detail as it has been particularly true of the condition prevailing in considered to be of great taxonomic utility the multituberculates at the subordinal level (Korvenkontio 1934). According to Koenigswald (Carlson and Krause 1985) and agrees well with the (1980), the acquisition of mul tiserial Hunter­ situation prevailing in the Rodentia and the Schreger bands in the incisors of various phylo­ Primates, the only two other mammalian orders that genetical ly unrelated forms; Vombatus have been studied in any detail in this regard. (Marsupialia); Daubentonia (Primates); Myotragus Rodents are at present one of the best and Hippotragus (Artiodacty~a); and in_the studied examples of such a conformity: the two hystricomorph rodents is a functional adaptation. extant rodent enamel patterns, the multiserial (most hystricognaths) and the uniserial (myomorphs Materials and Methods and sciurornorphs) are clearly derivable from the pauciserial condition of the Early Tertiary The material on which the present study is rodents (Sahni 1980, 1984, 1985). When examined based was obtained from several sources:­ in greater detail, however, obvious discrepancies Professor RE Sloan, University of Minnesota at are seen to arise: the pauciserial condition is Minneapolis, provided a generous sample of the Bug found in al 1 Early Tertiary rodents even within Creek Ant hi 11 micrommal s of age. those families, for instance the Ctenodactylidae These include the multituberculates, Mesodma, and the Ischyromyidae which in the latter part of , , Stygimys and ; the Upper Tertiary acquired a multiserial and a the marsupial, ; the insectivores, uniserial enamel structure, respectively. The and Gypsonictop and the condylarthran, abruptness of this change from the pauciserial to Protungulatum. Professor TK Roy Chowdhary of the the extant rodent enamel conditions may either be Geological Studies Unit, Indian Statistical a signature of inadequate palaeontological samp- Institute, Calcutta, loaned samples of Triassic 1 ing during the Oligo-Miocene, or may reflect thecodonts and traversodontid from the modifications of the muscle stresses generated in Gondwana Pranhita-Godavari Basin of peninsular the cranial and mandibular structure of hystrico­ India for enamel ultrastructure work. The other morphous and sciurognathous rodents. Wi1 son material investigated here is from the author's own (1972) postulated that the changeover to the uni­ collection through field trips made in the Subathu serial condition preceded the modifications of formation of the Jammu Himalaya (Lower to Middle musculature, a viewpoint supported by Emry and Eocene), the Berwali Series of Kutch of the same Thorington (1982) on the basis of their study of age, the Neogene deposits around Pinjor (Siwal iks Protosciurus, the most ancient squirrel known. of Haryana) and Srinagar (Karewas of Kashmir). Wood (1980, 1985), on the other hand, considered Several micrographs of each taxon were taken that the changing muscle tensions brought about at the Institut Palaontologie, Bonn, on a the transition of the multi and uniserial enamel Cambridge 5-4 Scanning Electron Microscope (SEM) structure. instrument with facilities provided by Professor Similarly for the primates, Boyde and Martin HK Erben, Director, and funding through a Fellow­ (1982, 1984) have demonstrated a subordinal or ship of the Alexander Von Humboldt Foundation, superfamilial distinction as far as the enamel West Germany. Additional work was undertaken at structure of fossil and Recent primates is the SEM Laboratories, Centre of Advanced Study in concerned. Geology, Panjab University, Chandigarh, on a JEOL­ JSM-25S. Enamel Evolution in Fossil Reptiles and Mammals The taxa include several isolated thecodont prisms in theropod enamel from various teeth; and from the widespread localities throughout the world (Upper Gondwana Pranhita-Godavari Basins of peninsular Jurassic of Thailand; Early Cretaceous of Tunisia India; uncatalogued isolated teeth of Eozostrodon and the Late Cretaceous of Canada) has recently from Pant, Wales, presented to the Museum of been recorded, (Buffetaut et al. 1986). These Geology, Panjab University; Late Cretaceous findings suggest that the distinction between al lotherians, metatherians, and eutherians from reptilian and mammalian enamels is less obvious the Bug Creek Anthills of ; fossil than was previously considered, and that the ziphodont and recent crocodiles; rhinoceratoids, classical theory concerning the reptile-mammalian tapi raids, art iodacty ls and archaeocetes from the enamel evolution may have to be revised in the Eocene of Kashmir and Kutch; Eocene ctenod­ light of occurrence of prismatic enamel in some acty lids, African phiomyids, Siwalik murids, non-occluding, mul tireplacement dentitions. These rhizomyids, and primates (adapids and aspects had previously been discussed by Grine ramapithecines); and Karewa arvicolids. (1978) on the basis of his studies on Diademodon All fossil specimens were cleaned using an and Eozostrodon. ultrasonic vibrator and then etched with 2% HN □ 3 Poole (1957) considered that the transition for 8 to 10 sec, or with 0.5 HCL for 3 to 5 sec from the non-prismatic enamel structure of most and were immediately washed and cleaned in an reptiles to the prismatic condition of most ultrasonic vibrator to remove etching precipitates mammals, to be a relatively simple step which can (salts of chloride, nitrate etc.) which tend to be accomplished by the greater deepening of the build up on prism boundaries and other less etched Tomes Processes. The fact that some reptiles do areas. Small specimens which had to be sectioned have a prismatic structure raises the question in a specific orientation were first embedded in that what, if anything, do these reptiles have in an araldite-based plastic, heated in an oven for common? Two factors, enamel thickness and wear 12 hours at 4 □ 0 c and then ground and polished as through occlusion have been cited as important in desired. the development of prismatic enamel. At present, the answer to this problem is difficult to deter­ Evolutionary Aspects mine: in Uromastyx, the prismatic structure was ascribed by Cooper and Poole (1973) to the Though descriptive accounts of various specialized nature of the dentition which remains mammalian enamels are found in the literature for in occlusion in contrast to the condition in most well over a century (Tomes 1849, 1850), one of the multireplacement type reptilian teeth. However, earliest to consider the evidence of the fossil there are certain exceptions to the general, and record was Korvenkontio (1934). Thereafter, as apparently rational, principle of Poole (1957) interest in the subject gained ground, the that thick enamelled, occluding dentitions pro­ evolutionary aspects were pioneered in large moted the development of prisms. Sahni (1985) measure by Poole (1956, 1957, 1967) and Moss pointed out that not all therapsids that have (1969). The work of Poole (1956, 1957) is espe­ occluding dentitions have prismatic enamels. cially significant as it sought to document the Similarly, if the report of prismatic enamel in reptilian to mammalian enamel transition, not only crocodiles and theropod is correct, then by considering comparative amelogenesis in recent the factor of occlusion is not a necessary species of the two Classes, but also by taking prerequisite for the evolution of prismatic into account the fossil material. The structure. Furthermore, the Jurassic mammals of evolutionary features of enamel structure of the Family did not possess prismatic diverse and Tertiary vertebrates were enamels even though their teeth have undergone highlighted by Moss (1969) by optical microscopy, wear by occlusion (Moss 1969; Fosse et al. 1985). and reviewed by Osborn and Hillman (1979). Many At present no well documented data exists on this of the observations made by Moss (1969) have been critical period of mammalian history even though modified by studies on the SEM (Fosse et al. 1973, our knowledge of Jurassic mammals has increased 1978; Sahni 1979). considerably (Lil legraven et al. 1979). The enamel of a Triassic thecodont from the Reptilian Enamels (Fossil and Recent) Pranhita-Godavari Basin is illustrated here (Fig. 1) to show the features characteristic of most Using optical methods, Poole (1956, 1957) fossil and recent reptilian enamels. The enamel demonstrated that normal reptilian enamel has a is usually thin, with pronounced incremental lines uniform, parallel orientation of the hydroxy­ running throughout the thickness of the enamel. apatite crystallites perpendicular to the deve­ In most prismatic enamels, the incremental lines loping surface. He postulated that prism forma­ are usually discernible in those areas (usually tion in mammals resulted from prolonged occlusion, the external layer of interprismatic enamel) where accompanied by greater enamel thickness, and the prisms are not developed. Enamel tubules may or l □ cation of stress points (prisms) generated by may not be present. masticatory activity. The non-prismatic condition In crocodiles, even by optical methods, a was considered to be the typical reptilian wavy, non-parallel orientation of the hydroxy­ condition until Cooper and Poole (1973) demon­ apatite crystallites was noticed by earlier strated the presence of Pattern I prisms in workers and was termed "Saul eng l i ede rung" ( Pao le Uromastyx, an agamid lizard. Since then few 1956). Kumar (1983) recorded prismatic enamel other additional reports of prismatic reptilian (Type One Prisms) in serrated tooth crocodiles enamel have been published (Grine et al. 1979; (Cf. Pristichampsus) from the Subathu Formation of Buffetaut et al. 1986). The presence of Pattern I India. However, subsequent work on the material

1905 A. Sahni from the same locality showed that the majority of the uncertain interpretation of pre-prismatic teeth assigned to Pristichampsus did not have enamel by light microscopy (Moss 1969; Osborn and prismatic enamels. No reason can be ascribed to Hillman 1979), only those fossil specimens will this discrepancy except to comment that different be mentioned that have been studied by electron types of crocodiles may have been sampled which microscopy. are impossible to differentiate on the basis of The whose affinities to both the isolated material. In this connection, it is reptiles and mammals are as yet uncertain, have interesting to note the discovery of prismatic been studied for their tooth enamel structure by alligator enamel made by Y Dauphin (Lab. Frank et al. (1984). The teeth referable to the Paleontologie, Paris VI University, pers. comm. E genera and Haramiya are small, cuspate, Buff etaut). occlusally worn, and are considered to be The presence of prismatic enamel was observed ancestral to the multituberculates. Scanning in the extremely thin enamel of the tooth of a few electron microscopy of these teeth day old hatchling of the gangetic gavial, Gavialis suggests a preprismatic structure. A similar gangeticus, (Fig. 2). The specimen was obtained condition was noticed in the from the Kukrai l Crocodile Farm, Lucknow, in therian (Sigogneau-Russell et al. connection with a project dealing with morphometry 1984). In another recent study on the micro­ of developing crania of those crocodiles that had structure of multituberculate enamel, Fosse et al. died prematurely. The teeth for study were (1985) also investigated the teeth of primitive dissected out of a having a length of 8.5 therians, including the plagiaulacoids and the cm. docodontids. These mammals were also found to The enamel has a uni form thickness ranging possess preprismatic enamel. from about 45 to 60 JJm. Prisms are represented by The report of prismatic enamel in Eozostrodon circular, cylindrical rods, traversing the whole (Grine and Cruickshank 1978) is significant in the thickness of the enamel (Fig. 2). The differen­ context of its geological antiquity and suggests tiation into interprismatic and prismatic phases that in eotherians, prism structure evolved at the is quite distinct. The structure is extremely same time as the development of mammalian dental simplified and resembles that known for Uromastyx. structure. The structure of Eozostrodon enamel as No enamel tubules have been observed. It should described by Grine and Cruickshank (1978) has been be noted that a large sample of gavial hatchlings confirmed by Sahni (1985). could not be obtained subsequently for detailed study as the species is on the National Mammalian Enamels Conservation List. Furthermore, only certain transverse and sagittal sections showed the pris­ The best sampled primitive mammals are those matic structure. In other sections the structure from the Bug Creek Anthills of Montana from the was not clear either as a result of preparation, Late Cretaceous. These enamels, which were con­ artefact, or variation within the teeth. In adult temporaries of the dinosaurs, had already diff­ teeth of Gavialis, both fossil and recent, the erentiated into 3 well established subclasses: prismatic structure could not be observed. (multituberculates), (mar­ Therapsids are mammal-like reptiles that supials) and (placentals). Al 1 these developed a number of mammalian features by the groups are represented by di verse genera with a end of the Triassic period. Their dentition, herbivorous, omnivorous or insectivorous diet. therefore, deserves special attention as this The placentals were represented by the Orders group of animals may hold the key to the problem Insectivora, Condylarthra and Primates. of prismatic enamels. Although a number of genera have been studied by means of light microscopy Cretaceous (Moss 1969; Osborn and Hillman 1979) as well as by electron microscopy (Grine 1978; Grine et al. The characteristics of multituberculate 1979; Sahni 1985), the enamel stucture is not well enamel have been comprehensively studied by understood. There appears to be a wide structural several workers, the latest account being that of range from tubular, non-prismatic, pre-prismatic Carlson and Krause (1985) and Fosse et al. (1985) and prismatic enamels (Pat tern l prisms). Grine and the reference contained therein. Basically, et al. (1979) demonstrated the existence of prisms multituberculates have distinct prism patterns at in the South African therapsid repile, the subordinal level: the Ptilodonoidea are rep­ , while was found to be resented by small-sized Pattern l prisms similar non-prismatic. In an earlier study the related in many respects to contemporary eutherian enamels transversodontid Diademodon was also shown to be of Cimolestes and except for the fact non-prismatic (Grine 1978). Similarly, Sahni that ptilodontoids have tubular enamel. The (1985) found prismatic structure in Indian Taeniolabioidea, on the other hand, are traversodontid cynodonts, which are presently characterized by larger (prism diameters greatest generically indeterminable because the studied known for all mammals) pattern 3 prisms, also with sample was comprised only of isolated teeth (Fig. numerous enamel tubules. Sahni (1985) had 3). The traversodontids are associated with 2 suggested that in some taeniolabidoids, such as dicynodont genera known from the Triassic of Stygimys, the prism structure may not be strictly peninsular India, namely Wadiasaurus and homologous to Pattern 3 known in some living Rechnisaurus (Chatterjee et al. 1969). mammalian Orders. However, this suggestion has At present, there are no detailed studies on still to be examined in greater detail. Pattern 2 preprismatic (pseudo prismatic) enamel, even prisms form a small component in multituberculate though this transitional phase was one of the most enamel& Layering is not a common feature of most important in the evolution of enamel. In view of multituberculates, but it is a distinct feature of

7906 Enamel Evolution in Fossil Reptiles and Mammals

Fig. 1. Transverse section of Triassic thecodont tooth, Gondwana of Pranhita-Godavari Basin, peninsular India; enamel with prominent incremental lines.

the incisor (Sahni 1979). Transverse sections of fig. 2. Sagittal section of tooth enamel of the incisors of Mesodma show layering with an gavial hatchling showing differentiation into inner zone of elongated prisms inclined incisally. cylindrical rod-like prisms and interprismatic This structure represents one of the first areas. functional adaptations of the incisors to biomechanical stresses (Fig. 4). In rodents, fig. 3. Section showing enamel-dentine junction though the structure is basically different, the with circular prisms in Triassic traversodonti.d layering and the incisal bending of the prisms is cynodont from the Gondwana of Pranhi ta-Godavari still retained. The multituberculates, which were Basin. the palaeocological counterparts of the rodents, share with the latter group the condition in which fig. 4. Transverse section of Mesodma (Late the incisor structure was far removed from that of Cretaceous ptilodontid multituberculate) showing the molars. layering and bending over of prisms as a first The presence of tubules in the enamel, stage of differentiation (probably functional) particularly in the Taeniolabidoidea, has been between incisors and molars.

1907 A. Sahni noticed by all workers who have studied multi­ Hunter-Schreger bands (Fig. 7). Recent odono­ tuberculate enamel. These occur in the prismatic cetes, on the other hand, lack well developed as well as in the interprismatic phases and are in zonation, but otherwise have a similar structure direct continuation with the dentinal tubules. to the archaeocetes. Sma11 er odontocetes tend to No systematic study has yet been undertaken have more mineralized, better developed prismatic on the enamel of fossil marsupials apart from the enamel than the larger-sized toothed whales work done on the light microscope (Moss 1969). (Ishiyama 1984). Preliminary work done on the Alphadon from There are interesting functional implications the Bug Creek Anthill Hill locality indicates a involved in the evolution of the enamel of rhino­ structure similar to that known for recent ceroses and lophodont ungulates (Rensberger and marsupials (Sahni 1979). However, detailed Koenigswald 1980; Fortelius 1984). Rensberger and evolutionary trends must await further Koenigswald (1980) have shown that the Hunter­ investigations. Schreger bands in some Early to Middle Eocene Of the Bug Creek eutherians, the enamel lophodont perissodactyls (eg., the rhinoceratoids) structure has been worked out only for the were oriented horizontally and underwent a full insectivores Cimolestes and Gypsonictops and the 90° reorientation as evolution progressed in this condylarhran Protungulatum. The primate group. The vertical orientation of the Hunter­ Purgatorius known from this horizon has yet to be Schreger bands is considered to impart to the investigated, (Sloan and Van Valen 1965). The lophs greater resistance to wear. Similar condi­ Late Cretaceous insectivores seem to have under­ tions of functional adaptation have been described gone little modification in respect to their for other lophodont ungulates including the modern counterparts which have Pattern l prisms Miocene suid Listriodon (Fortelius 1984). (Sahni 1979). Protungulatum, on the other hand, The record of enamel ultrastructure evo­ considered by consensus opinion to be ancestral to lution in rodents is becoming clearer through the most ungulates, possesses both Pattern l and works of Koenigswald (1980, 1985), Sahni (1980, Pattern 3 prisms. The latter pattern can be 1985), Hussain et al. (1978) and De Bruijn et al. observed in Fig. 5 where the roughly hexagonal (1982). The evolution in canid () markings corresponding to the secretory enamels was undertaken by Reif (1974) while that territories of the ameloblasts can be seen along in proboscideans by Kozawa (1978). The enamel with the open-sided prisms boundaries. This type ultrastructure of a Middle Eocene rodent and of preservation is rather uncommon in the fossil ungulate assemblage from the Lesser Himalaya of record. India was described by Kumar (1983). The enamel structure of the prototherians is Tertiary and Recent another fascinating subject which is just getting the attention that it deserves. Recently, Lester The Tertiary was a period of great radiation and Boyde (1986) have shown that Ornithorhynchus lea ding to the present diversity of mammals. The has prismatic enamel in part, but that this is not first systematic documentation of Recent mammalian a primary feature of living enamel. ultrastructure was undertaken by Boyde (1964) who Incremental lines and other radial features are laid down the foundation of evolutionary studies more readily apparent. Lester and Archer (J.986) of the enamel structure of modern eutherian in their study of the Middle Miocene monotreme lineages. A beginning has thus been made in Obduron have shown, on the other hand, that this recording enamel evolution in most mammalian taxon possesses prismatic tubular enamel. Pattern orders (Kozawa 1984). Important aspects of l predominates in the innermost enamel, while a documentation include the description of the prism Pattern 2 packing occurs in the middle third, the structure and the functional responses of the outermost enamel is non-prismatic. On the basis enamel structure of Tertiary and Recent lineages of the similarity of a number of enamel features wherever there has not been a radical structural between and multituberculates, these modification. authors speculate on the possibility of a Recently, a great deal of attention has been monphyletic origin for both these groups, a paid to primate enamel evolution, particularly in hypothesis which needs to be examined in greater the context of primitive hominoids, (Gantt et al., detail. 1977; Gantt 1980, 1983; Vrba and Grine 1978; Sahni et al. 1983; Boyde and Martin 1984). Preliminary Future Challenges findings by Boyde and Martin (1984) suggest that Pattern l, found in all Lemuriformes, may be The interest aroused during the last decade considered as the most generalized for all in fossil vertebrate mineralized tissue has led to Primates, implying thereby that Pattern 2 and 3 a better understanding of the taxonomic diversity enamels represent derived conditions within the and evolutionary significance of the dental order, and to distinguish the cercopi theoids histology of reptiles and mammals (Table 1). The within that suborder. The structure of a Miocene future lines of investigation clearly fall into 3 Siwalik adapid primate wih predominantly Pattern 3 categories:- first, to have a better understanding packing is shown in Fig. 6. of the reasons (functional or otherwise) of the Cetacean enamel evolution has been studied by exception to the general enamel structure of a Sahni (1981) and Ishiyama (1984). These studies particular group; eg., the absence of tubules in suggest that in the Middle Eocene when primitive Vombatus, the presence of a non-prismatic, tubular whales (archaeocetes) had large, functional and enamel in the cetacean Phoconoides, the loss of occlusal ly worn teeth, the enamel structure was zones in most odontocetes, etc. Second, is the clearly prismatic (Pattern 1) with a well detailed documentation of enamel structure of differentiated Von Korff layer and distinct those fossil lineages which are we11 established Enamel Evolution in Fossil Reptiles and Mammals

Table 1. Geochronological distribution of enamel structure in enamel of fossil reptiles and mammals. I T E RT I A R Y I RECENT TRIAS I JURASSIC ICRETACEOUS IPALEOGENEINEOGENEIPLEISTOCENE 180my l)Omy 65my ZSmy I .8my R xx , } E OIAOEMOOON,ETC. TRAUERSODONT DICYNODONT p I PACHYGENELUS 1 T ------THEROPOD DINOSAUR I o o o HARAMYIDAE L ? ___ ? PLACODONTIA E s ?_ ~ --? ZIPHODONT CROC. UROMASTYX I ------?-- ORNITHORHYNCHUS( PROTOTHERIAI M o K UHNEOTHERIUM A o o o DOCODONTIDAE M o o PL AGIAULACIDAE ) M PTILODONTDIDEA!:.-.____ IT______MULTITUBERCULATA TAENIOLABIDOIDEA••--- _l!.J_T_~_ - - --- A -Ii: _ EOZOSTRODON PAPPOTHERIIOAE LEGEND GYPSONICTOPS_I,]_ • • • • •INSECTIVORA _I CIMOLESTES_ I__ x NON PRISMATIC A o PRE PRISMATIC PROTUNGULATUM- ~ - • • •• UNGULATES ' - PRISMATIC EURYMYLIDAE _?£' ~ PZ l·J PRISM PATTERN G GIGANTO PRISM RODENTIA r-----~'--ti-- --­ P PAUCISERIAL - I__ ARCHAEOCETES M MULTISERIAL CETACEA ( ODONTOCETES". - - _,_ - - - - - U UNISERIAL PROBOSCIOEA __ ~ ____ _ T TUBULES Z ZONATION CARNIVORA __ ) _ ___ _ •••PRESUMED LEMURIFORMES _ '-.- ANCESTRY CERCOPITHECIDAE_ £ PRIMATES { AOAPIOAE _) _ HOMINIDS ____ J__ _ PEDIOMYS 2T MARSUPIALS ... ~T- __

on the basis of gross dental morphology and skeletal anatomy to analyse the reasons for similarities or discrepancies at the ultrastuctural level. Lastly, it is necessary to find out common factors for those reptiles that do possess prismatic enamels and for those mammals that do not. The study of the evolution of enamel is still at the preliminary stage. Mesozoic reptiles and mammals hold the key in unravelling the complexities of enamel evolution.

Fig. 5. Transversely sectioned enamel of Protungulatum (Late Cretaceous ancestral ungulate from Montana) showing Pattern 3 prisms.

fig. 6. Horizontal section of the enamel of Si valadapis nag)ii (Adapidae, Primates, from the Indian Siwaliks showing typical Pattern 3 prisms.

Fig. 7. Transverse section of enamel of primitive whale (Eocene archaeocete from Kutch, India) showing Hunter-Schreger Bands and Pattern l prisms. A differentiated Von Korff zone is present at the outer dentinal layer.

7909 A. Sahni References Frank RM, Sigogneau-Russel l D & Vogel JC (1984) Tooth ultrastructure of Late Triassic Haramiyidae. Boyde A (1964) The structure and development J. Dent. Res. 63: 661-664. of mammalian enamel. PhD Thesis, University of London. Gantt DG, Pilbeam DR & Steward GP (1977) Hominoid enamel prism patterns. Sci. 198: 1155- Boyde A & Martin L (1982) Enamel Microstructure 1157. Determination in Hominoid and Cercopi thecoid Primates. Anat. Embryol. 165: 193-212. Gantt DG (1980) Implications of enamel prism patterns. Scanning Electron Microsc. 1979; 11: Boyde A & Martin L (1984) A non-destructive 491-496. survey of enamel prism packing pattern in primate enamel. In: Tooth Enamel IV, Proc. Elsevier Sci. Gantt DG (1983) The enamel of Neogene Publ. BV Amsterdam. (Eds) Fearnhead RW, Suga S: hominoids: structural and phyletic implications. 417-421. In: New Interpretations of the Age and Hunman Ancestry. Ciochon RL, Corrucini RS (Eds) Plenum, Buffetaut E, Dauphin Y, Jaeger JJ, Martin M, New York: 249-298. Mazin JM & Tong H (1986) La structure de l 'email dentaire chez les Reptiles: presence de prismes Grine FE & Cruickshank ARI (1978) Scanning chez les Dinosaures theropodes. CR Acad. Sci. Electron Microscope analysis of postcanine tooth Paris 302(11): 979-982. structure in the Late Triassic mammal Eozostrodon (Eotheria: Triconodonta) Proc. Electron Mier. Carlson SJ & Krause OW (1985) Enamel Ultra­ Seo. S. Afr. 8: 121-122. structure of Multituberculate mammals. An Investigation of Variability. Contrib. Mus. Grine FE (1978) Postcanine dental structure in Palaeontol. Univ. Michigan. 27(1): 1-50. Mammal-like reptile Diademodon (Therapsida: Cynodonta). Proc. Electron Mier. Soc. S. Afr. 8: Chatterjee S, Jain SL, Kutty TS & Roychowdhury 123-124. TK (1969) On the discovery of Triassic Cynodont reptiles from India. Sci. & Culture 35: 411-416. Grine FE, Gow CE & Kitching JW (1979). Enamel structure in the cynodonts. Proc. Electron Mier. Cooper JS & Poole DFG (1973) The dentition and Soc. S. Afr. 9: 99-100. dental tissues of the agamid lizard, Uromastyx. J. Zool. 169: 85-100. Hussain ST, De Bruijn H & Leinders JM (1978) Middle Eocene rodents from the Kala Chitta Range De Bruijn H, Hussain ST & Leinders JJM (1982) On (Punjab, Pakistan). Proc. Kon Nederl. Akad. West. some Early Eocene rodent remains from Barbara Amsterdam Ser. B, Bl: 74-112. Banda, Kohat, Pakistan, and the early history of the order Rodentia. Proc. Kon. Nederl. Akad. Wet. Ishiyama M (1984) Comparative histology of Ser. B 85(3): 249-258. tooth enamel in several toothed whales. In: Tooth Enamel IV, Proc. Elsevier Sci. Publ. BV Fearnhead Emry RJ & Thorington RW (1982) Descriptive and RW, Suga S (Eds): 432-436. comparat1ve osteology of the oldest fossil squirrel, Protosciurus (Rodentia: Sciuridae). Koenigswald WV (1980) Schmelzstruktur und Smithsonian Contrib. Palaeobiol. 47: 1-35. Morphologie in den Mclaren der Arvicolidae (Rodentia). Abn. Senckenb. Naturforsch. Ges. 539: Flynn LJ (1982) Variability of incisor enamel 1-129. microstructure within Gerbil l us. J. Mamm. 63(1): 162-165. Koenigswald WV (1985) The use of Enamel struc­ ture in Evaluating the Relationships among Higher Fortelius M (1984) Vertical decussation of Categories of Rodents. NATO-CNRSRodent Phylogeny enamel prisms in lophodont ungulates in Tooth Symp. Paris. Luckett P, Hartenberger JL (Eds) Enamel IV. Proc. Elsevier Sci. Publ. BV Plenum Press New York Ser. A 92: 403-422. Amsterdam. (Eds) Fearnhead RW, Suga S: 427- 431. Korvenkontio VA (1934) Mikroskopische Untersuchungen an Nagerincisiven unter Hinweis auf Fosse G, Eskidsen O, Risnes S & 51 oan RE (1978) die Schmel zstruktur der Backenzahne. Ann. Zool. Prisms size in tooth enamel of some Late Soc. Zool. Bot. Fenn. Vanamo 2: 1-274. Cretaceous mammals and its value in mul tituber­ culate . Zool. Scripta. z: 57-61. Kozawa Y (1978) Comparative histology of probo­ scidean molar enamel. J. Stoma to l. Soc. Japan 45: Fosse G, Kielan-Jaworowska Z & Skaale SG (1985) 585-606. The Microstructure of tooth enamel in Multituber­ culate mammals. Palaeontology 28(3): 435-449. Kozawa Y (1984) The development of evolution of mammalian enamel structure. In: Tooth Enamel IV Fosse G, Risnes S & Holmbakken M (1973) Prisms Proc. Elsevier Sci. Publ. VB Fearnhead RW, Suga S and tubulex in multituberculate enamel. Cal. (Eds): 437-441. Tiss. Res. 11: 133-150. Enamel Evolution in Fossil Reptiles and Mammals

Kumar K (1983) Palaeontological & palaeohisto­ Sahni A, Tewari BN & Kumar K (1983) A report on logical Investigations of Subathu Vertebrates from the occurrence of Ramapithecus punjabicus Jammu & Kashmir & Himachal Pradesh. Unpublished (Hominoidea) from the Ut tar Pradesh Siwa l iks. Him. PhD Thesis, Panjab University, Chandigarh. Geol. Sem. (1980). Proc. WIHG Dehradun 11: 193- 197. Lester KS & Boyde A (1986) Scanning Microscopy of teeth. Anat. Embryo 1. 174: 15-26. Sigogneau-Russell D, Frank RM & Hemmerle J (1984) Enamel and dentine ultrastructure in Early Lester KS & Archer M (1986) A description of Jurassic therian Kuehneotherium. In: Patterson C. the molar enamel of a Middle Miocene Montoreme Commemorative volume of Professor KA Kermack. (, Ornithorhynchidae). Anat. Embryol. Zool. Jl. Linn. Soc. Londo.n 82: 207-215. 174: 145-151. Sloan R & Van Valen L (1965) Late Cretaceous Lillegraven JA, Kielan-Jawarowska Z & Clemens WA Mammals from Montana. Sci. 148(3667): 220-227. (1979) Mesozoic Mammals, University California. Press, Berkeley: 1-311. Tomes J (1849) On the structure of the dental tissues of marsupial animals and especially of the Moss ML (1969) Evolution of mammalian dental enamel. Phil. Trans. Roy. Soc. London 139: 403- enamel. Amer. Mus. Novit. 2360: 1-39. 412.

Osborn JW & Hillman J (1979) Enamel Structure Tomes J (1850) On the structure of the dental in some therapsids & Mesozoic Mammals. Cal. Tiss. tissues of the Order Rodentia. Phil. Trans. Roy. Int. 29: 47-61. Soc. London 140: 529-567.

Poole DFG (1956) The structure of the teeth of Vrba ES & Grine FE (1978) Australopithecine some mammal-like reptiles. Quart. J. Mier. Sci. enamel prism patterns. Sci. 202: 890-892. 97: 303-312. Wilson RW (1972) Evolution and in Poole DFG (1957) The formation & properties of Early Tertiary Rodents. Proc. 24th Int. Geol. the Organic Matrix of reptilian tooth enamel. Congr. Harpells Press Cooperative, Gardenvale, Quart. J. Mier. Sci. 98: 349-367. Quebec, 7: 217-224.

Poole DFG (1967) Enamel Structure in primitive Wood AE (1980) The Oligocene Rodents of North mammals. J. Dent. Res. 46: 124. America. Trans. Amer. Philos. Soc. 70: 1-68.

Reif WE (1974) REM-Beobachtungen am Schmelz lvood AE (1985) Origin, dispersal and evolut­ eines rezenten und eines fossilen Caniden. ionary relationships of the hystricognath rodents. Biomin. 7: 56-69. NATO-CNRS. Rodent Phylogeny Symp. Paris. Luckett PW, Hartenberger JL (Eds). Plenum Press, New York Rensberger JM & Koenigswald WV (1980) Ser. A, 92: 475-514. Functional & Phylogenetic interpretation of enamel microstructure in rhinoceroses. Paleobiol. 6(4): Discussion with Reviewers 477-495. -- Reviewer III: There is a growing amount of Sahni A (1979) Enamel structure in certain controversy concerning discrete types of enamel North American Cretaceous mammals. Palaeonto- structure, particularly relating to the graphica A, 166: 37-49. categories: nonprismatic, preprismatic, pseudo­ prismat ic. Can you, based on your work on Sahni A (1980) SEM studies of Indian Eocene & specimen of taxa at your disposal, clarify this Siwalik rodent enamels. Geosci. J. 1: 21-30. confusion? Author: My observations are: some hatchling Sahni A (1981) Ultrastructure of fossil gavials did have prismatic enamel, others did not. Mammalia: Eocene Archaeoceti from Kutch. J. The same applies to studies of fossil rep ti 1 ian Paleontol. Soc. India 25: 33-37. enamel where Buffetaut et al. (1986) found prismatic enamel in some theropod (carnivorous Sahni A (1984) The evolution of mammalian dinosaur) teeth from the Cretaceous of Canada, enamels: evidence from Multituberculate Jurassic of Thailand, etc. Also, Yannick Dauphine (Allotheria, extinct); primitive whales has recorded prismatic enamel in alligator enamel. (Archaeocete cetacea) & Early rodents. Tooth I feel that these reports are significant and Enamel IV. Proc. Elsevier Sci. Publ. BV Amsterdam would motivate scientists to intensify their Fearnhead RW, Suga S (Eds): 457-461. research along these lines. It is true that right now we do not fully know why some taxa have Sahni A (1985) Enamel structure of Early prismatic enamel and others do not. Mammals and its role in evaluating relationships amongst rodents - Sym. Proc. Luckett PW, Reviewer III: You state that multituberculates Hartenberger JL (Eds) Plenum & Co. Evolutionary have Pattei:n 1 and Pattern 3 prisms. In your 1979 Analysis of Rodents, NATO-CNRSSer. A 92: 133-150. paper (p. 41), you state that "the principal ar­ rangement of prisms conforms to Pattern 1 ... with a few oblique, horizontal and longitudinal

l 9 l l A. Sahni sections showing Pattern 2. Contrary to findings of Fosse et al. (1973), Pattern 3 appears to be minimal or even absent". In your 1985 paper (p. 140), you refer to the prism arrangement in Stygimys, a taeniolabidoid, as "a modified version of Pattern 3," that is, it is not "strictly homologous to Pattern 3 prisms". Now, you refer to them as Pattern 3 prisms with no qualification or explanation of why they are not Pattern 2 or a modified Pattern 3. Which theory are we to believe? Author: In 1979, when I published in Palaeonto­ graphica, there were very few papers on SEM application to fossil dental enamel. The dominant pattern that I recognized then for the multituber­ culates was Pattern l (with small amounts of Pat­ tern 2). I failed to identify Pattern 3. In my 1985 paper (by which time a number of scientists had taken up this work and the general knowledge on the structure of fossil dental enamel was better), I revised my earlier opinion and considered both Pattern land 3 to be the predomi­ nant patterns in the Ptilodontoidea and the Taeniolabidoidea, respectively.

Reviewer II I: You 1 ist teeth of Eozostrodon as among thosethat were examined in the course of this study, yet no mention is made of Eozostrodon in the rest of the paper except to say that Grine et al. (1979) examined its enamel structure. Eozostrodon is crucial to our understanding of the early evolution of mammalian enamel. Did you find the same structure as did Grine et al.? You also list several other higher taxa that were apparently examined during the course of this study. What were your findings? Author: Yes, I did find the same structure in Eozostrodon as reported by Grine and Cruickshank.

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