Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics

Relative warp analyses of landmarks describing cranial and mandibular shape are used for investigating patterns of morphological variation among extant bears (Mammalia, Carnivora, Ursidae) indicative of diet and feeding behavior. These patterns are used for deriving inferences about the autecology of two extinct species previously assumed to have had different dietary preferences, the North American giant, short-faced bear Arctodus simus and the Eurasian cave bear Ursus spelaeus . Results reveal a set of shared craniodental traits among the herbivorous bears, including short and vaulted skulls with well-developed zygomatic arches, lateralized orbits and small canines, concave jaws with a highly positioned condyle, large moment arms for the temporalis and masseter muscles, and long cheek teeth. In contrast, those bears that consume animal resources have long skulls with small zygomatic arches, frontalized orbits and well-developed canines, and long jaws with a deep mandibular symphysis, low muscle leverages, a condyle situated at the level of the tooth row and reduced cheek teeth. The craniodental morphology of omnivorous bears is intermediate between those of faunivores and herbivores. This is also the case of the short-faced bear and the cave bear, which suggests that previous reconstructions of the feeding ecology of these extinct species (highly carnivorous for A. simus and herbivorous for U. spelaeus ) should be revised.     

The relationship between diet and tooth complexity in living dentigerous saurians

Living saurian reptiles exhibit a wide range of diets, from carnivores to strict herbivores. Previous research suggests that the tooth shape in some lizard clades correlates with diet, but this has not been tested using quantitative methods. I investigated the relationship between phenotypic tooth complexity and diet in living reptiles by examining the entire dentary tooth row in over 80 specimens comprising all major dentigerous saurian clades. I quantified dental complexity using orientation patch count rotated (OPCR), which discriminates diet in living and extinct mammals, where OPCR‐values increase with the proportion of dietary plant matter. OPCR was calculated from high‐resolution CT‐scans, and I standardized OPCR‐values by the total number of teeth to account for differences in tooth count across taxa. In contrast with extant mammals, there appears to be greater overlap in tooth complexity values across dietary groups because multicusped teeth characterize herbivores, omnivores, and insectivores, and because herbivorous skinks have relatively simple teeth. In particular, insectivorous lizards have dental complexities that are very similar to omnivores. Regardless, OPCR‐values for animals that consume significant amounts of plant material are higher than those of carnivores, with herbivores having the highest average dental complexity. These results suggest reptilian tooth complexity is related to diet, similar to extinct and extant mammals, although phylogenetic history also plays a measurable role in dental complexity. This has implications for extinct amniotes that display a dramatic range of tooth morphologies, many with no modern analogs, which inhibits detailed dietary reconstructions. These data demonstrate that OPCR, when combined with additional morphological data, has the potential to be used to reconstruct the diet of extinct amniotes. J. Morphol. 278:500–522, 2017. © 2017 Wiley Periodicals, Inc.     

Postcranial morphology and the locomotor habits of living and extinct carnivorans

Members of the order Carnivora display a broad range of locomotor habits, including cursorial, scansorial, arboreal, semiaquatic, aquatic, and semifossorial species from multiple families. Ecomorphological analyses from osteological measurements have been used successfully in prior studies of carnivorans and rodents to accurately infer the locomotor habits of extinct species. This study uses 20 postcranial measurements that have been shown to be effective indicators of locomotor habits in rodents and incorporates an extensive sample of over 300 individuals from more than 100 living carnivoran species. We performed statistical analyses, including analysis of variance (ANOVA) and stepwise discriminant function analysis, using a set of 16 functional indices (ratios). Our ANOVA results reveal consistent differences in postcranial skeletal morphology among locomotor groups. Cursorial species display distal elongation of the limbs, gracile limb elements, and relatively narrow humeral and femoral epicondyles. Aquatic and semiaquatic species display relatively robust, shortened femora and elongate metatarsals. Semifossorial species display relatively short, robust limbs with enlarged muscular attachment sites and elongate claws. Both semiaquatic and semifossorial species have relatively elongate olecranon process of the ulna and enlarged humeral and femoral epicondyles. Terrestrial, scansorial, and arboreal species are characterized by having primarily intermediate features, but arboreal species do show relatively elongate manual digits. Morphological indices effectively discriminate locomotor groups, with cursorial and arboreal species more accurately classified than terrestrial, scansorial, or semiaquatic species. Both within and between families, species with similar locomotor habits converge toward similar postcranial morphology despite their independent evolutionary histories. The discriminant analysis worked particularly well to correctly classify members of the Canidae, but not as well for members of the Mustelidae or Ursidae. Results are used to infer the locomotor habits of extinct carnivorans, including members of several extinct families, and also 12 species from the Pleistocene of Rancho La Brea. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

The impact of digging on craniodental morphology and integration

The relationship between the form and function of the skull has been the subject of a great deal of research, much of which has concentrated on the impact of feeding on skull shape. However, there are a number of other behaviours that can influence craniodental morphology. Previous work has shown that subterranean rodents that use their incisors to dig (chisel‐tooth digging) have a constrained cranial shape, which is probably driven by a necessity to create high bite forces at wide gapes. Chisel‐tooth‐digging rodents also have an upper incisor root that is displaced further back into the cranium compared with other rodents. This study quantified cranial shape and upper incisors of a phylogenetically diverse sample of rodents to determine if chisel‐tooth‐digging rodents differ in craniodental morphology. The study showed that the crania of chisel‐tooth‐digging rodents shared a similar place in morphospace, but a strong phylogenetic signal within the sample meant that this grouping was nonsignificant. It was also found that the curvature of the upper incisor in chisel‐tooth diggers was significantly larger than in other rodents. Interestingly, most subterranean rodents in the sample (both chisel‐tooth and scratch diggers) had upper incisors that were better able to resist bending than those of terrestrial rodents, presumably due to their similar diets of tough plant materials. Finally, the incisor variables and cranial shape were not found to covary consistently in this sample, highlighting the complex relationship between a species’ evolutionary history and functional morphology.     

Regulation of tooth number by fine-tuning levels of receptor-tyrosine kinase signaling

Much of our knowledge about mammalian evolution comes from examination of dental fossils, because the highly calcified enamel that covers teeth causes them to be among the best-preserved organs. As mammals entered new ecological niches, many changes in tooth number occurred, presumably as adaptations to new diets. For example, in contrast to humans, who have two incisors in each dental quadrant, rodents only have one incisor per quadrant. The rodent incisor, because of its unusual morphogenesis and remarkable stem cell-based continuous growth, presents a quandary for evolutionary biologists, as its origin in the fossil record is difficult to trace, and the genetic regulation of incisor number remains a largely open question. Here, we studied a series of mice carrying mutations in sprouty genes, the protein products of which are antagonists of receptor-tyrosine kinase signaling. In sprouty loss-of-function mutants, splitting of gene expression domains and reduced apoptosis was associated with subdivision of the incisor primordium and a multiplication of its stem cell-containing regions. Interestingly, changes in sprouty gene dosage led to a graded change in incisor number, with progressive decreases in sprouty dosage leading to increasing numbers of teeth. Moreover, the independent development of two incisors in mutants with large decreases in sprouty dosage mimicked the likely condition of rodent ancestors. Together, our findings indicate that altering genetic dosage of an antagonist can recapitulate ancestral dental characters, and that tooth number can be progressively regulated by changing levels of activity of a single signal transduction pathway.     

Skeletal indicators of locomotor adaptations in living and extinct rodents

Living rodents show great diversity in their locomotor habits, including semiaquatic, arboreal, fossorial, ricochetal, and gliding species from multiple families. To assess the association between limb morphology and locomotor habits, the appendicular skeletons of 65 rodent genera from 16 families were measured. Ecomorphological analyses of various locomotor types revealed consistent differences in postcranial skeletal morphology that relate to functionally important traits. Behaviorally similar taxa showed convergent morphological characters, despite distinct evolutionary histories. Semiaquatic rodents displayed relatively robust bones, enlarged muscular attachments, short femora, and elongate hind feet. Arboreal rodents had relatively elongate humeri and digits, short olecranon processes of the ulnae, and equally proportioned fore and hind limbs. Fossorial rodents showed relatively robust bones, enlarged muscular attachments, short antebrachii and digits, elongate manual claws, and reduced hind limb elements. Ricochetal rodents displayed relatively proximal insertion of muscles, disproportionate limbs, elongate tibiae, and elongate hind feet. Gliding rodents had relatively elongate and gracile bones, short olecranon processes of the ulnae, and equally proportioned fore and hind limbs. The morphological differences observed here can readily be used to discriminate extant rodents with different locomotor strategies. This suggests that the method could be applied to extinct rodents, regardless of ancestry, to accurately infer their locomotor ecologies. When applied to an extinct group of rodents, we found two distinct ecomorphs represented in the beaver family (Castoridae), semiaquatic and semifossorial. There was also a progressive trend toward increased body size and increased aquatic specialization in the giant beaver lineage (Castoroidinae). J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Dietary adaptations in the teeth of murine rodents (Muridae): a test of biomechanical predictions

Functional dental theory predicts that tooth shape responds evolutionarily to the mechanical properties of food. Most studies of mammalian teeth have focused on qualitative measures of dental anatomy and have not formally tested how the functional components of teeth adapt in response to diet. Here we generated a series of predictions for tooth morphology based on biomechanical models of food processing. We used murine rodents (Old World rats and mice) to test these predictions for the relationship between diet and morphology and to identify a suite of functional dental characteristics that best predict diets. One hundred and five dental characteristics were extracted from images of the upper and lower tooth rows and incisors for 98 species. After accounting for phylogenetic relationships, we showed that species evolving plant‐dominated diets evolved deeper incisors, longer third molars, longer molar crests, blunter posteriorly angled cusps, and more expanded laterally oriented occlusal cusps than species adapting to animal‐dominated diets. Measures of incisor depth, crest length, cusp angle and sharpness, occlusal cusp orientation, and the lengths of third molars proved the best predictors of dietary adaptation. Accounting for evolutionary history in a phylogenetic discriminant function analysis notably improved the classification accuracy. Molar morphology is strongly correlated with diet and we suggest that these dental traits can be used to infer diet with good accuracy for both extinct and extant murine species.     

Cranial anatomy and palaeobiology of the Miocene marsupial Hondalagus altiplanensis and a phylogeny of argyrolagids

New cranial material of Hondalagus altiplanensis, from the middle Miocene of southern Bolivia, allows a rediagnosis of the genus and an assessment of its palaeobiology and phylogenetic relationships with other argyrolagid marsupials. The new specimens demonstrate several derived (synapomorphic) cranial features shared by HondalagusArgyrolagus: a globular braincase, ventrally directed occipital condyles, a broad zygomatic arch, and a short, deep dentary with a flat and long coronoid notch. Hondalagus had powerful masticatory muscles and its cementum-encased hypselodont cheek teeth suggests it had a very abrasive diet. The deep fossae on the lateral aspect of the skull of argyrolagids, interpreted by Simpson as large, laterally-facing orbits, are actually sharply margined temporal fossae. Hondalagus has a very large carotid foramen medially situated within the suture of the basisphenoid and basioccipital. A phylogenetic analysis of five argyrolagid genera was conducted using 32 characters (16 cranial, 16 dental) and a didelphid and a caenolestid as outgroups. Hondalagus-Argyrolagus-Microtragulus form a monophyletic group with an undescribed gen. et sp. nov. (MACN-Ch-1305) from the lower Miocene (Colhuehuapian) of Argentina as its sister taxon. Proargyrolagus appears as sister group to the other taxa of argyrolagids.     

On the Scaling of Tooth Size in Mammals

We must establish the allometric regularities of functionalscalingin interspecific, "mouse-to elephant" plots in orderto provide criteria for the recognition of special adaptationsunrelated to the requirements of size. The qualitative literaturesuggests that postcanine tooth areas of herbivorous mammalsshould increase with positive allometry in such plots. Thispositive allometry might reflect the demands of metabolism orthe ecological strategies of large vs. small hervivores embodiedin Levins' concept of environmental grain. Plots of postcaninearea vs. body size display the expected postive allometry inall groups studied: hystricomorph rodents, suine artiodactyls(pigs, peccaries, and hippos), cervoid artiodactyls (deer, s.l),and four groups of primates considered separately (lemuroids,ceboids, cercopithecoids, and great apes). Sketchy data foraustralopithecines also indicate positive allometry and therelatively larger cheek teeth of robust forms may only reflecttheir larger body size and not the dietary differences so oftenadvocated. Phyletic dwarfs of large herbivores display negativeallometry (relatively larger cheek teeth in dwarfs) in oppositionto the interspecific trend.     

The Skull of Stephanomys and a Review of Malpaisomys Relationships (Rodentia: Muridae): Taxonomic Incongruence in Murids

The cranial morphology of the extinct murid genus Stephanomys, previously known only by dental remains, is described here on the basis of partial skulls of three species of Pliocene age. Important cranial characters of the genus are a robust rostrum, a high zygoma, a wide zygomatic arch, a narrow interorbit, a large orbit, and an optic foramen in the backward position. In addition to some dental characters, Stephanomys shares most of these cranial traits with the extinct Malpaisomys from the Canary Islands. Some of these traits may be linked to the development of large eyes and life in a rocky environment. The peculiar dental pattern of Stephanomys (stephanodonty) is also present in some recent murids (Oenomys and Thamnomys) having a different skull morphology. A comparison with nine other extant genera of murids verified the relationship among Malpaisomys, Stephanomys, and Acomys, supporting our previous conclusion. Phenetic and cladistic analyses of 17 cranial and 23 dental characters show that skull morphology is phylogenetically informative but highly convergent and incongruent with other partial evidence based on dental and biochemical characters. The combined analyses of skull and teeth illustrate a case of mosaic evolution in murids.     

Morphology and postnatal ontogeny of the cranial endocast and paranasal sinuses of capybara (Hydrochoerus hydrochaeris), the largest living rodent

Recent studies have analyzed and described the endocranial cavities of caviomorph rodents. However, no study has documented the changes in the morphology and relative size of such cavities during ontogeny. Expecting to contribute to the discussion of the endocranial spaces of extinct caviomorphs, we aimed to characterize the cranial endocast morphology and paranasal sinuses of the largest living rodent, Hydrochoerus hydrochaeris, by focusing on its ontogenetic growth patterns. We analyzed 12 specimens of different ontogenetic stages and provided a comparison with other cavioids. Our study demonstrates that the adult cranial endocast of H. hydrochaeris is characterized by olfactory bulbs with an irregular shape, showing an elongated olfactory tract without a clear circular fissure, a marked temporal region that makes the endocast with rhombus outline, and gyrencephaly. Some of these traits change as the brain grows. The cranial pneumatization is present in the frontal and lacrimal bones. We identified two recesses (frontal and lacrimal) and one sinus (frontal). These pneumatic cavities increase their volume as the cranium grows, covering the cranial region of the cranial endocast. The encephalization quotient was calculated for each specimen, demonstrating that it decreases as the individual grows, being much higher in younger specimens than in adults. Our results show that the ontogenetic stage can be a confounding factor when it comes to the general patterns of encephalization of extinct rodents, reinforcing the need for paleobiologists to take the age of the specimens into account in future studies on this subject to avoid age-related biases.     

Dental and cranial variation in living Indriidae

Four species of Indriidae are extant in Madagascar. We have studied large samples of each of these to characterize dental and cranial variation, and to estimate the degree of sexual dimorphism in the dentition and cranium. Two dental fields are apparent, characterized by reduced variability: (1) a canine field centered on the upper canine and occluding caniniform lower premolar, and (2) a cheek tooth field centered on the second molars. No consistent pattern of sexual dimorphism was found in dental or cranial dimensions, and we conclude that none of the four species is sexually dimorphic. This lack of dental and cranial dimorphism is unusual in primates, and probably reflects the relatively limited aggressive behavior and the lack of male dominance in Indriidae.     

Nuciruptor rubricae,a new Pitheciin seed predator from the Miocene of Colombia

A new genus and species of platyrrhine primate, Nuciruptor rubricae, are added to the increasingly diverse primate fauna from the middle Miocene of La Venta, Colombia. This species displays a number of dental and gnathic features indicating that it is related to living and extinct Pitheciinae (extant Callicebus, Pithecia, Chiropotes, Cacajao, and the Colombian middle Miocene Cebupithecia sarmientoi). Nuciruptor is markedly more derived than Callicebus but possesses a less derived mandibular form and incisor-canine complex than extant and extinct pitheciins (Cebupithecia, Pithecia, Chiropotes, and Cacajao), suggesting that it is a primitive member of the tribe Pitheciini within the larger monophyletic Pitheciinae. Nuciruptor has procumbent and moderately elongate lower incisors and low-crowned molars, suggesting that it was a seed predator, as are living pitheciins. Its estimated body size of approximately 2.0 kg places it within the size range of extant pitheciines. The dental and gnathic morphology of Nuciruptor clarifies several aspects of dental character evolution in Pitheciinae and makes it less likely that the enigmatic Mohanamico hershkovitzi (m. Miocene, Colombia) is a pitheciin. Am. J. Phys. Anthropol. 102:407–427, 1997. © 1997 Wiley-Liss, Inc.     

Reconstruction of the cranial musculature and masticatory function of the Pleistocene panamerican ground sloth Eremotherium laurillardi (Mammalia,Xenarthra, Megatheriidae)

Cranial musculature, dental function and mandibular movement patterns in Eremotherium laurillardi were reconstructed from the examination of crania and dentitions. Size, shape and pattern of muscle divisions were reconstructed from the examination of bony rugosities indicating muscle attachments. Details of masticatory muscle structure and function were based on dissections of the tree sloths Bradypus and Choloepus. Among sloths, masticatory muscles in E. laurillardi demonstrate a different synergist–antagonist pattern, reflecting greater emphasis on mediolateral mandibular movements. Eight cranial character complexes (anterior facial, zygomatic arch, superficial masseter, deep masseter–zygomaticomandibularis, pterygoid, temporal, occipital and occlusal) determined by interrelated contributions of each component made to group functions were identified. An elongate anterior face and predental spout in E. laurillardi allowed protrusion of a long narrow tongue at small degrees of gape, reflecting a probably ancestral xenarthran condition. Gape minimisation, in conjunction with the mediolaterally directed masticatory stroke in E. laurillardi, was a unique solution to increase masticatory efficiency by permitting molariform tooth shearing surfaces to remain in or near occlusion for a greater percentage of each chewing cycle.     

A reassessment of the cranial morphology of Neoepiblema acreensis (Rodentia: Chinchilloidea), a Miocene rodent from South America

The rodent Neoepiblema acreensis (Chinchilloidea: Neoepiblemidae) is member of a lineage that reached gigantic dimensions during the Late Miocene of South America—the Neoepiblemidae. In this paper, the cranial anatomy of this rodent is reviewed. Noninvasive imaging is used to reveal internal structures. Our review is based mainly on an almost complete cranium from the Upper Miocene deposits of the western Amazonia of Brazil. The cranium has an elongated rostrum, large frontal sinuses, a deep temporal fossa, well-developed sagittal, nuchal, medial occipital, and secondary crests, and a tympanic fenestra connected to the external acoustic meatus by a thin ventral cleft. Remarkably, the cranium shows the presence of fossae on the posterior region of the frontal and parietal bones, and a “W-shaped” fronto-parietal suture, which are not present in other analyzed chinchilloids. This study contributes to the knowledge of the morphology of this extinct rodent as well as to the phylogenetic relationships and paleobiology of neoepiblemids.     

Regional ultrastructural and cytochemical comparisons of the epithelial-mesenchymal interface during rat incisor development

A major theme in understanding epithelial-mesenchymal interactions during development focuses upon regional mesenchyme specification of epithelial differentiation. One particularly useful epidermal organ system for studying this issue is the rodent continuously growing and erupting incisor tooth organ. One advantage of this particular system resides in the regional features of the rodent incisor tooth organ. Along the labial surface, inner dental epithelial cells differentiate into ameloblasts that produce enamel extracellular matrix, whereas the epithelia along the lingual surface do not become ameloblasts and do not produce enamel matrix. This study has been designed to compare ultrastructural features of labial versus lingual surfaces, with particular emphasis upon mesenchymal cell shape, the orientation of extracellular matrix collagen, the basal lamina, and the distribution of sulfated glycoconjugates. Critical analyses of the data indicated that different microenvironments exist between epithelia and mesenchyme in the labial versus the lingual surfaces of the developing rodent incisor tooth organ.     

The impact of digging on the evolution of the rodent mandible

There are two main (but not mutually exclusive) methods by which subterranean rodents construct burrows: chisel-tooth digging, where large incisors are used to dig through soil; and scratch digging, where forelimbs and claws are used to dig instead of incisors. A previous study by the authors showed that upper incisors of chisel-tooth diggers were better adapted to dig but the overall cranial morphology within the rodent sample was not significantly different. This study analyzed the lower incisors and mandibles of the specimens used in the previous study to show the impact of chisel-tooth digging on the rodent mandible. We compared lower incisors and mandibular shape of chisel-tooth digging rodents with nonchisel-tooth digging rodents to see if there were morphological differences between the two groups. The shape of incisors was quantified using incisor radius of curvature and second moment of area (SMA). Mandibular shape was quantified using landmark based geometric morphometrics. We found that lower incisor shape was strongly influenced by digging group using a Generalized Phylogenetic ancova (analysis of covariance). A phylogenetic Procrustes anova (analysis of variance) showed that mandibular shape of chisel-tooth digging rodents was also significantly different from nonchisel-tooth digging rodents. The phylogenetic signal of incisor radius of curvature was weak, whereas that of incisor SMA and mandibular shape was significant. This is despite the analyses revealing significant differences in the shape of both mandibles and incisors between digging groups. In conclusion, we showed that although the mandible and incisor of rodents are influenced by function, there is also a degree of phylogenetic affinity that shapes the rodent mandibular apparatus.     

Factors influencing the distributional abundance of two trophic guilds of Peruvian cricetid rodents

The distributional abundance of 13 species of southern Peruvian rodents is significantly correlated with altitude and patterns of vegetation but vegetation is a better predictor than altitude. Coincidental reversals in the altitudinal trends of both vegetation and rodents demonstrate that rodents are responding to vegetation patterns. Abundance and diversity of rodents are greatest around 4000 m elevation which coincides with the region of greatest vegetational abundance and seasonally heavy rainfall.
The rodent communities consist of two separate feeding guilds, omnivores and insectivores and these guilds show distinctly different distributional patterns. Insectivorous species are strongly associated with the zone of seasonally heavy rainfall (4000 m) whereas omnivorous rodents are relatively abundant over a broader spectrum of elevations and habitats. In a previous study of these same communities, we showed a correspondence between rodent morphology and their diets. This study reveals a correspondence between distributional abundance of the various species and their diets. We conclude that the distributional abundance of southern Peruvian rodents is related to the physiological constraints imposed by altitude (climate) and the distributional abundance of food resources.     

Incisor microwear of Sumatran anthropoid primates

Several studies have suggested that incisor microwear reflects diet and feeding adaptations of anthropoids. However, such studies have been largely qualitative, and interpretations have relied on anecdotal references to diet and tooth use reported in the socioecology literature. The current study relates incisor microwear in four anthropoid primates to specific ingestive behaviors and food types. Central incisor casts of wild-shot museum specimens of Hylobates lar, Macaca fascicularis, Pongo pygmaeus, and Presbytis thomasi were examined by scanning electron microscopy, and analyzed using a semiautomated image analysis procedure. Microwear patterns were used to generate predictions regarding diet and anterior tooth use. These predictions were evaluated using data collected during a 1 year study of feeding behavior of these same taxa in the wild (Ungar, 1992, 1994a, b). Results suggest that (1) enamel prism relief is associated with the effectiveness of etching reagents in foods, (2) dental calculus buildup results from a lack of incisor use and perhaps the ingestion of sugar-rich foods, (3) striation density varies with degree of anterior tooth use in the ingestion of abrasive food items, (4) striation breadth is proposed to relate to the ratio of exogenous grit to phytoliths consumed; and (5) preferred striation orientation indicates the direction that food items are pulled across the incisors during ingestion. It is concluded that incisor microwear studies can contribute to the understanding of diets and feeding behaviors of extinct primates. © 1994 Wiley-Liss, Inc.