Convergence analysis of a finite element skull model of Herpestes javanicus (Carnivora, Mammalia): implications for robust comparative inferences of biomechanical function.

Predictions of skull biomechanical capability based on virtual models constitute a valuable data source for testing hypotheses about craniodental form and feeding behavior. Such comparative analyses also inform dietary reconstruction in extinct species. 3D modeling using Finite Element (FE) methods is a common technique applied to the comparative analysis of craniodental function in extinct and extant vertebrates. However, taxonomically diverse skull models in the literature often are not directly comparable to each other, in part because of distinctions in how boundary conditions are defined, but also because of substantial differences in the number of FEs composing the models. In this study, we test whether a conventional convergence test is adequate in identifying the minimum number of FEs needed to achieve internally stable results for a single species. We constructed a series of skull models of Herpestes javanicus, and simulated unilateral biting across the dentition; the models differed in the number of FEs, degrees of freedom at the joint and bite point constraints, and type of tetrahedral FEs used. We found that convergence patterns differed across constraint types, FE quantities, and bite position simulated. Four-noded tetrahedral (tet-4) FE models with relaxed constraints produced the most stable measurements compared to over-constrained tet-4 models and to relaxed tet-10 models. In absence of an optimal FE quantity from convergence testing, we propose a broadly applicable sub-sampling protocol, whereby average measurement values across multiple models per specimen are used for among-species comparisons. A regime of sampling three low FE quantity models produced the closest estimates of mean measurement values relative to larger model sets, being within the 95% bootstrap estimated confidence intervals. Future studies should focus on identifying sources of variation associated with other FE modeling protocols, so that they can be accounted for before biomechanical attributes from these simulations are used to infer form-function linkage.

Locomotive implication of a Pliocene three-toed horse skeleton from Tibet and its paleo-altimetry significance.

The Tibetan Plateau is the youngest and highest plateau on Earth, and its elevation reaches one-third of the height of the troposphere, with profound dynamic and thermal effects on atmospheric circulation and climate. The uplift of the Tibetan Plateau was an important factor of global climate change during the late Cenozoic and strongly influenced the development of the Asian monsoon system. However, there have been heated debates about the history and process of Tibetan Plateau uplift, especially the paleo-altimetry in different geological ages. Here we report a well-preserved skeleton of a 4.6 million-y-old three-toed horse (Hipparion zandaense) from the Zanda Basin, southwestern Tibet. Morphological features indicate that H. zandaense was a cursorial horse that lived in alpine steppe habitats. Because this open landscape would be situated above the timberline on the steep southern margin of the Tibetan Plateau, the elevation of the Zanda Basin at 4.6 Ma was estimated to be ∼4,000 m above sea level using an adjustment to the paleo-temperature in the middle Pliocene, as well as comparison with modern vegetation vertical zones. Thus, we conclude that the southwestern Tibetan Plateau achieved the present-day elevation in the mid-Pliocene.

From 'third pole' to north pole: a Himalayan origin for the arctic fox.

The 'third pole' of the world is a fitting metaphor for the Himalayan-Tibetan Plateau, in allusion to its vast frozen terrain, rivalling the Arctic and Antarctic, at high altitude but low latitude. Living Tibetan and arctic mammals share adaptations to freezing temperatures such as long and thick winter fur in arctic muskox and Tibetan yak, and for carnivorans, a more predatory niche. Here, we report, to our knowledge, the first evolutionary link between an Early Pliocene (3.60-5.08 Myr ago) fox, Vulpes qiuzhudingi new species, from the Himalaya (Zanda Basin) and Kunlun Mountain (Kunlun Pass Basin) and the modern arctic fox Vulpes lagopus in the polar region. A highly hypercarnivorous dentition of the new fox bears a striking resemblance to that of V. lagopus and substantially predates the previous oldest records of the arctic fox by 3-4 Myr. The low latitude, high-altitude Tibetan Plateau is separated from the nearest modern arctic fox geographical range by at least 2000 km. The apparent connection between an ancestral high-elevation species and its modern polar descendant is consistent with our 'Out-of-Tibet' hypothesis postulating that high-altitude Tibet was a training ground for cold-environment adaptations well before the start of the Ice Age.

Three-dimensional computer simulations of feeding behaviour in red and giant pandas relate skull biomechanics with dietary niche partitioning.

The red (Ailurus fulgens) and giant (Ailuropoda melanoleuca) pandas are mammalian carnivores convergently adapted to a bamboo feeding diet. However, whereas Ailurus forages almost entirely on younger leaves, fruits and tender trunks, Ailuropoda relies more on trunks and stems. Such difference in foraging mode is considered a strategy for resource partitioning where they are sympatric. Here, we use finite-element analysis to test for mechanical differences and similarities in skull performance between Ailurus and Ailuropoda related to diet. Feeding simulations suggest that the two panda species have similar ranges of mechanical efficiency and strain energy profiles across the dentition, reflecting their durophagous diet. However, the stress distributions and peaks in the skulls of Ailurus and Ailuropoda are remarkably different for biting at all tooth locations. Although the skull of Ailuropoda is capable of resisting higher stresses than the skull of Ailurus, the latter is able to distribute stresses more evenly throughout the skull. These differences in skull biomechanics reflect their distinct bamboo feeding preferences. Ailurus uses repetitive chewing in an extended mastication to feed on soft leaves, and Ailuropoda exhibits shorter and more discrete periods of chomp-and-swallow feeding to break down hard bamboo trunks.

Whence the beardogs? Reappraisal of the Middle to Late Eocene 'Miacis' from Texas, USA, and the origin of Amphicyonidae (Mammalia, Carnivora).

The Middle to Late Eocene sediments of Texas have yielded a wealth of fossil material that offers a rare window on a diverse and highly endemic mammalian fauna from that time in the southern part of North America. These faunal data are particularly significant because the narrative of mammalian evolution in the Paleogene of North America has traditionally been dominated by taxa that are known from higher latitudes, primarily in the Rocky Mountain and northern Great Plains regions. Here we report on the affinities of two peculiar carnivoraforms from the Chambers Tuff of Trans-Pecos, Texas, that were first described 30 years ago as Miacis cognitus and M. australis. Re-examination of previously described specimens and their inclusion in a cladistic analysis revealed the two taxa to be diminutive basal amphicyonids; as such, they are assigned to new genera Gustafsonia and Angelarctocyon, respectively. These two taxa fill in some of the morphological gaps between the earliest-known amphicyonid genus, Daphoenus, and other Middle-Eocene carnivoraforms, and lend additional support for a basal caniform position of the beardogs outside the Canoidea. The amphicyonid lineage had evidently given rise to at least five rather distinct forms by the end of the Middle Eocene. Their precise geographical origin remains uncertain, but it is plausible that southern North America served as an important stage for a very early phase of amphicyonid radiation.

Are cranial biomechanical simulation data linked to known diets in extant taxa? A method for applying diet-biomechanics linkage models to infer feeding capability of extinct species.

Performance of the masticatory system directly influences feeding and survival, so adaptive hypotheses often are proposed to explain craniodental evolution via functional morphology changes. However, the prevalence of "many-to-one" association of cranial forms and functions in vertebrates suggests a complex interplay of ecological and evolutionary histories, resulting in redundant morphology-diet linkages. Here we examine the link between cranial biomechanical properties for taxa with different dietary preferences in crown clade Carnivora, the most diverse clade of carnivorous mammals. We test whether hypercarnivores and generalists can be distinguished based on cranial mechanical simulation models, and how such diet-biomechanics linkages relate to morphology. Comparative finite element and geometric morphometrics analyses document that predicted bite force is positively allometric relative to skull strain energy; this is achieved in part by increased stiffness in larger skull models and shape changes that resist deformation and displacement. Size-standardized strain energy levels do not reflect feeding preferences; instead, caniform models have higher strain energy than feliform models. This caniform-feliform split is reinforced by a sensitivity analysis using published models for six additional taxa. Nevertheless, combined bite force-strain energy curves distinguish hypercarnivorous versus generalist feeders. These findings indicate that the link between cranial biomechanical properties and carnivoran feeding preference can be clearly defined and characterized, despite phylogenetic and allometric effects. Application of this diet-biomechanics linkage model to an analysis of an extinct stem carnivoramorphan and an outgroup creodont species provides biomechanical evidence for the evolution of taxa into distinct hypercarnivorous and generalist feeding styles prior to the appearance of crown carnivoran clades with similar feeding preferences.

Using a Novel Absolute Ontogenetic Age Determination Technique to Calculate the Timing of Tooth Eruption in the Saber-Toothed Cat, Smilodon fatalis.

Despite the superb fossil record of the saber-toothed cat, Smilodon fatalis, ontogenetic age determination for this and other ancient species remains a challenge. The present study utilizes a new technique, a combination of data from stable oxygen isotope analyses and micro-computed tomography, to establish the eruption rate for the permanent upper canines in Smilodon fatalis. The results imply an eruption rate of 6.0 millimeters per month, which is similar to a previously published average enamel growth rate of the S. fatalis upper canines (5.8 millimeters per month). Utilizing the upper canine growth rate, the upper canine eruption rate, and a previously published tooth replacement sequence, this study calculates absolute ontogenetic age ranges of tooth development and eruption in S. fatalis. The timing of tooth eruption is compared between S. fatalis and several extant conical-toothed felids, such as the African lion (Panthera leo). Results suggest that the permanent dentition of S. fatalis, except for the upper canines, was fully erupted by 14 to 22 months, and that the upper canines finished erupting at about 34 to 41 months. Based on these developmental age calculations, S. fatalis individuals less than 4 to 7 months of age were not typically preserved at Rancho La Brea. On the whole, S. fatalis appears to have had delayed dental development compared to dental development in similar-sized extant felids. This technique for absolute ontogenetic age determination can be replicated in other ancient species, including non-saber-toothed taxa, as long as the timing of growth initiation and growth rate can be determined for a specific feature, such as a tooth, and that growth period overlaps with the development of the other features under investigation.

Testing adaptive hypotheses of convergence with functional landscapes: a case study of bone-cracking hypercarnivores.

Morphological convergence is a well documented phenomenon in mammals, and adaptive explanations are commonly employed to infer similar functions for convergent characteristics. I present a study that adopts aspects of theoretical morphology and engineering optimization to test hypotheses about adaptive convergent evolution. Bone-cracking ecomorphologies in Carnivora were used as a case study. Previous research has shown that skull deepening and widening are major evolutionary patterns in convergent bone-cracking canids and hyaenids. A simple two-dimensional design space, with skull width-to-length and depth-to-length ratios as variables, was used to examine optimized shapes for two functional properties: mechanical advantage (MA) and strain energy (SE). Functionality of theoretical skull shapes was studied using finite element analysis (FEA) and visualized as functional landscapes. The distribution of actual skull shapes in the landscape showed a convergent trend of plesiomorphically low-MA and moderate-SE skulls evolving towards higher-MA and moderate-SE skulls; this is corroborated by FEA of 13 actual specimens. Nevertheless, regions exist in the landscape where high-MA and lower-SE shapes are not represented by existing species; their vacancy is observed even at higher taxonomic levels. Results highlight the interaction of biomechanical and non-biomechanical factors in constraining general skull dimensions to localized functional optima through evolution.

Skull shape evolution in durophagous carnivorans.

In this article, we investigate convergent evolution toward durophagy in carnivoran skull shape using geometric morphometrics in a sample of living and extinct species. Principal components analysis indicate that, in spite of the different dietary resources consumed by durophages-that is, bone-crackers and bamboo-feeders-both groups of carnivorans share portions of skull phenotypic spaces. We identify by discriminant analyses a shared set of adaptations toward durophagy in the skull of carnivores. However, ancestral states indicate that although durophages reached similar phenotypes, the evolutionary pathways that they followed are different depending upon the family to which they belong. Furthermore, while the carnivoran cranium more closely reflects the nature of the resources consumed-that is, soft or hard and tough items-the mandible shows particular feeding adaptations-that is, bamboo or bone. This finding supports the interpretation that the mandible has more evolutionary plasticity than the cranium, which is more limited to evolve toward a particular feeding adaptation. However, we find that the shapes of the cranium and the mandible are highly integrated for the whole order Carnivora. Published studies of teratological cats and dogs indicate that the role of internal constraints in shaping this pattern of integration is absent or weak and malleable by selection.

Model sensitivity and use of the comparative finite element method in mammalian jaw mechanics: mandible performance in the gray wolf.

Finite Element Analysis (FEA) is a powerful tool gaining use in studies of biological form and function. This method is particularly conducive to studies of extinct and fossilized organisms, as models can be assigned properties that approximate living tissues. In disciplines where model validation is difficult or impossible, the choice of model parameters and their effects on the results become increasingly important, especially in comparing outputs to infer function. To evaluate the extent to which performance measures are affected by initial model input, we tested the sensitivity of bite force, strain energy, and stress to changes in seven parameters that are required in testing craniodental function with FEA. Simulations were performed on FE models of a Gray Wolf (Canis lupus) mandible. Results showed that unilateral bite force outputs are least affected by the relative ratios of the balancing and working muscles, but only ratios above 0.5 provided balancing-working side joint reaction force relationships that are consistent with experimental data. The constraints modeled at the bite point had the greatest effect on bite force output, but the most appropriate constraint may depend on the study question. Strain energy is least affected by variation in bite point constraint, but larger variations in strain energy values are observed in models with different number of tetrahedral elements, masticatory muscle ratios and muscle subgroups present, and number of material properties. These findings indicate that performance measures are differentially affected by variation in initial model parameters. In the absence of validated input values, FE models can nevertheless provide robust comparisons if these parameters are standardized within a given study to minimize variation that arise during the model-building process. Sensitivity tests incorporated into the study design not only aid in the interpretation of simulation results, but can also provide additional insights on form and function.

Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia).

Morphological specialization is a complex interplay of adaptation and constraint, as similarly specialized features often evolve convergently in unrelated species, indicating that there are universally adaptive aspects to these morphologies. The evolutionary history of carnivores offers outstanding examples of convergent specialization. Among larger predators, borophagine canids were highly abundant during the tertiary of North America and are regarded as the ecological vicars of Afro-Eurasian hyenas. Borophaginae is an extinct group of 60+ species, the largest forms evolving robust skulls with prominently domed foreheads, short snouts, and hypertrophied fourth premolars. These specializations have been speculated to enhance bone cracking. To test the extent that the skulls of derived borophagines were adapted for producing large bite forces and withstanding the mechanical stresses associated with bone cracking relative to their nonrobust sister clades, we manipulated muscle forces in models of six canid skulls and analyzed their mechanical response using 3D finite element analysis. Performance measures of bite force production efficiency and deformation minimization showed that skulls of derived borophagines Borophagus secundus and Epicyon haydeni are particularly strong in the frontal region; maximum stresses are lower and more evenly distributed over the skull than in other canids. Frontal strength is potentially coupled with a temporalis-driven bite to minimize cranial stress during biting in the two derived genera, as tensile stress incurred by contracting temporalis muscles is dissipated rostro-ventrally across the forehead and face. Comparison of estimated masticatory muscle cross section areas suggests that the temporalis-masseter ratio is not strongly associated with morphological adaptations for bone cracking in Borophagus and Epicyon; larger body size may explain relatively larger temporalis muscles in the latter. When compared with previous studies, the overall cranial mechanics of the derived borophagines is more similar to bone-cracking hyaenids and percrocutids than to their canid relatives, indicating convergence in both morphological form and functional capability.