From Head to Tail: New Models and Approaches in Primate Functional Anatomy and Biomechanics

Abstract

This special issue of The Anatomical Record (AR) is based on interest generated by a symposium at the 2008 annual meeting of the American Association of Anatomists (AAA) at Experimental Biology, entitled “An Evolutionary Perspective on Human Anatomy.” The development of this volume in turn provided impetus for a Biological Anthropology Mini-Meeting, organized by members of the AAA for the 2010 Experimental Biology meeting in Anaheim, California. The research presented in these pages reflects the themes of these symposia and provides a snapshot of the current state of primate functional anatomy and biomechanics research. The 17 articles in this special issue utilize new models and/or approaches to study long-standing questions about the evolution of our closest relatives, including soft-tissue dissection and microanatomical techniques, experimental approaches to morphology, kinematic and kinetic biomechanics, high-resolution computed tomography, and Finite Element Analysis (FEA). This volume continues a close historical association between the disciplines of anatomy and biological anthropology: anatomists benefit from an understanding of the evolutionary history of our modern form, and biological anthropologists rely on anatomical principles to make informed evolutionary inferences about our closest relatives. Anat Rec, 293:544–548, 2010. © 2010 Wiley-Liss, Inc.

The disciplines of anatomy and biological anthropology are closely linked: anatomists benefit from an understanding of the evolutionary history of our modern form, and biological anthropologists rely on anatomical principles to make informed evolutionary inferences about our closest relatives. This special issue of The Anatomical Record (AR) is the direct result of a symposium entitled “An Evolutionary Perspective on Human Anatomy,” held during the 2008 meeting of the American Association of Anatomists (AAA), at Experimental Biology, San Diego, California, 7 April 2008. The symposium was organized by the first author (JMO), and was co-sponsored by the AAA Advisory Committee for Young Anatomists. In that symposium, four articles were delivered on the comparative, functional, and evolutionary anatomy of the non-human primate skull, wrist, thoracic cage, and hip/thigh, followed by a discussion led by Jeffrey Laitman, president-elect of AAA and associate editor of AR. Given the resounding interest and attendance at this symposium, Jeff and AR-editor-in-chief Kurt Albertine strongly encouraged JMO to organize a special issue devoted to promote new models and approaches to primate functional anatomy, which brings this special issue to light. In turn, contributors to this issue created a critical mass of excellent research, providing a foundation for many of the symposia of the Biological Anthropology Mini-Meeting at the 2010 AAA meeting at Experimental Biology in Anaheim, California. The timing of publication of this special issue—April 2010—is intentional; this issue appears in print coincident with the Mini-Meeting, where a number of the authors in this issue are invited to share their research with a broader anatomy audience.

The title of this issue of AR is “From Head to Tail: New Models and Approaches in Primate Functional Anatomy and Biomechanics.” As the title suggests, the articles included in this volume utilize new approaches and methods to study comparative anatomical and biomechanical questions surrounding the evolution of our closest relatives, both living and extinct. Therefore, these articles represent a snapshot of the current state of primate functional anatomy and biomechanics research.

The research presented in the succeeding pages follows on the heels of over 45 years of major advances in research methodologies and knowledge, beginning with the 1965 symposium on primate locomotion convened by the late Warren Kinzey (Kinzey,1967). Kinzey's symposium was significant because it was the first to explicitly detail the evolution and function of one particular anatomical/functional complex, and from an experimental perspective [the “New Physical Anthropology”—Washburn (1951)]. Subsequent symposia have taken similar approaches, for example focusing on the functional anatomy and evolution of the postcranial primate skeleton and locomotion (e.g., Strasser and Dagosto,1988; Gebo,1993; Strasser et al.,1998) or primate craniofacial biomechanics (e.g., Vinyard et al.,2008). This special issue, and the symposium that generated it, takes a more holistic approach to primate functional anatomy research. Thus, we follow the example of other symposium proceedings focusing on multiple functional complexes and multiple methodologies to understand the functional anatomy of primates (e.g., Tuttle,1975; Anapol et al.,2004; Dominy et al.,2004). Specifically, the articles included in this issue are roughly equally divided among craniofacial studies and postcranial studies, and use methodologies ranging from soft-tissue dissection and microanatomical techniques to high-resolution microcomputed tomography and Finite Element Analysis (FEA) to understand anatomical adaptation and evolution in our closest relatives.

CRANIOFACIAL ANATOMY AND BIOMECHANICS

The first three articles in this issue examine the biomechanics of mastication and its relationship to anatomical form. Bucinell et al. (2010) empirically test the predictions of conventional curved beam theory in the analysis of Old World monkey mandibular structure. Using stereophotogrammetric methods (Digital Image Correlation), these authors convincingly demonstrate that the observed disparity between labial and lingual symphyseal stresses in colobines is reduced relative to a papionin, but that the patterns of stress distribution are not consistent with predictions based on an idealized curved beam model of mandibular architecture.

The contribution from Ravosa et al. (2010) provides the first comprehensive examination of the scaling of loading parameters in the masticatory complex in a diverse group of mammals varying in body size by over 2.5 orders of magnitude. Mandibular corpus strain data detailed here indicate that peak-strain magnitudes and occlusal duty factor during chewing are similar across mammals of varying body size, while chewing frequency is inversely correlated with body size. When compared against similar scaling analyses of locomotor loading parameters, the data presented here help illustrate a more complete picture of skeleton-wide patterning of osteogenic stimuli across many taxa.

A novel analysis by Vinyard and Taylor (2010) examines the correlation between masticatory muscle architecture and muscle recruitment patterns during chewing in primates. Masseter architecture is not correlated with muscle activity pattern, whereas temporalis architecture is correlated with muscle activity pattern. Thus, as primates recruit more of their balancing side superficial temporalis muscle during chewing, they are able to generate higher contraction forces in this muscle, suggesting that the architecture of these muscles evolved as separate functional units, which may be related to novel functional roles in divergent primate clades.

FEA, an innovative tool for examining how objects of complex design resist load using engineering techniques, has become a widely available tool for biological anthropologists and many other researchers (Ross,2005). Three articles in this volume use FEA to understand how craniodental morphology may be adapted to particular functional behaviors such as hard-object feeding or paramasticatory behaviors. Strait et al. (2010) investigate whether the derived mid-facial features in australopiths (early fossil humans) are adaptations to chewing hard objects on a regular basis. By isometrically scaling applied muscle forces to FE models of Macaca fascicularis and Australopithecus africanus, they demonstrate that the australopith craniofacial skeleton is structurally more rigid than that of the macaque, especially during premolar biting, which is consistent with hypotheses that A. africanus may have consumed large, hard food items.

Berthaume et al. (2010) employ a unique combination of physical (material properties) testing of artificial food items designed to simulate nuts and seeds, and finite element modeling of these food items, to examine the adaptation of hominin dentitions. Results indicate significant differences in fracture forces, displacements, and energies across food types and taxa, which are inconsistent with existing functional hypotheses of occlusal form. These authors present a new Strong Cusp Hypothesis, consistent with their findings, suggesting that tooth morphology of early hominins (and other hard object feeders) may not represent adaptations for inducing fractures in food items, but rather for resisting fractures of the tooth crown itself.

Even the mid-facial skeleton of more recent humans demonstrates a wide spectrum of variation often cited as adaptations to different environmental and mechanical selective pressures. The study by Wang et al. (2010) investigates the mechanical impact of incisor loading on the mid-facial skeleton using FEA. By carefully manipulating loads placed on the incisors at different degrees of mid-facial projection, these authors find that an anteroposteriorly shortened mid-face may be the most effective way to dissipate anterior occlusal forces. However, this morphology is not necessarily effective in combating various paramasticatory behaviors (as observed for Inuits and inferred for Neandertals).

Zeroing on core samples of bone, Dechow et al. (2010) examine the effects of tooth loss and reduced masticatory loading on facial cortical bone. They employ an ultrasonic technique to measure the material properties of maxillae and other regions of the facial skeleton. Compared to those of dentate skulls, edentate skulls have thinner cortices, with stiffer and less anisotropic bone, even in the supraorbital area normally under low masticatory stress. These results provide evidence that bone strain resulting from normal occlusal forces is important in maintaining bone tissue homeostasis, and is likely implicated as a factor behind development, variation, and evolution of the craniofacial skeleton.

Several articles in this volume employ computed tomography (CT), a non-invasive high resolution radiographic tool that is augmented by computer processing. This technique has become more widely available in the past decade, enabling internal access to skeletal structure, which was previously unprecedented without destructive sampling. Following on the themes of the preceding articles and taking an explicit experimental approach, Menegaz et al. (2010) also demonstrate adaptations in neurocranial morphology attributed to differential mechanical loading. In this case, these authors use three-dimensional morphometric methods and measurements derived from micro CT to evaluate the effects of differential masticatory loading on neurocranial form. They find that the neurocranium may respond to increased masticatory loading by increasing cranial vault thickness and/or altering the curvature of the cranial vault.

The article by Jašarević et al. (2010) explores the mechanical properties of soft-tissue structures of the circumorbital region in rabbits raised on diets of differing consistency. In this microanatomical study, the authors find that increased masticatory stresses incurred with a more fracture-resistant diet are correlated with a more degraded organization of collagen fibers in postorbital ligament (and fibrocartilage). Along the lateral orbital wall, elastic fibrocartilage, not ligament, is observed. In light of the lack of marked changes in the extracellular composition of the lateral orbital wall related to tissue viscoelasticity, Jašarević et al. (2010) suggest it is unlikely that long-term exposure to elevated masticatory stresses underlies the development of the bony postorbital bar and the evolution of a postorbital bar in primates from the postorbital ligament (the primitive condition for mammals).

Employing both micro CT and histological methods, Smith et al. (2010) examine the extent of fusion of a facial suture in two species of adult bushbabies. Their results indicate that sutures which appear externally patent can be internally fused or indirectly “tethered” via fusion to underlying bones. Since patent sutures function, in part, to redistribute mechanical forces in adjacent bones, these findings have potentially important implications for the study of craniofacial biomechanics. Smith et al. (2010) assert that micro CT is a useful tool for studying suture mechanics, and discuss its unique suite of advantages and limitations when compared to more traditional methods such as serial sectioning for histology.

POSTCRANIAL ANATOMY AND BIOMECHANICS

Two articles in this special issue examine the effects of increased mechanical loading on joint articular shape, using very different approaches. The first of these articles, by Hammond et al. (2010), characterizes the macro- and microanatomical responses of the femoral growth plate, articular cartilage, and bone in juvenile swine subjected to different locomotor activity patterns. They find that compared to articular cartilage, the growth plate demonstrates higher response to mechanical loading and bears greater adaptive changes, in which chondrocyte hypertrophy and proliferation are more important factors in chondral modeling than certain aspects of the extracellular matrix. This suggests area- and type- specific responses in cartilage modeling during ontogeny.

The contribution from Sylvester and Organ (2010), the second of these articles, examines the intraspecific scaling of laser-scanned three-dimensional articular joint shape in the medial tibial condyle of large-bodied hominoids. Like the Hammond et al. (2010) contribution, this study does not find allometric shape differences in articular surfaces within species. However, these results are based on adult animals, and do not address the ontogeny of articular surface shape as does the Hammond et al. (2010) contribution. Nevertheless, this study finds no support for hypotheses of joint flattening with increased transarticular loading related to body size.

Taking a more classical approach to the study of primate functional anatomy, Wright-Fitzgerald et al. (2010) investigate for the first time the soft-tissue structures of the shoulder joint in prosimians with a diverse array of locomotor and postural behaviors. They demonstrate various adaptation scenarios which may have occurred during the evolutionary history of these primates, including relative changes in overall muscle mass coincident with locomotor strategies, the presence or absence of individual ligaments, and different morphologies of individual articular surfaces. The thrust of Wright-Fitzgerald et al.'s arguments indicate that while the soft-tissue joint morphologies of these prosimians may be less adaptive than osseous morphology to locomotor and postural behaviors, the knowledge of soft-tissue structure greatly enriches our understanding of shoulder anatomy, function and evolution.

The relationship between mobility of individual carpal bones and overall wrist mobility is difficult to describe two-dimensionally due to the complexity of the joints in question. To address such issues, Orr et al. (2010) present a novel markerless registration method to extract motion axis parameters from conventional CT that describe bone movements during normal wrist motions. The application of this method to studies of primate evolutionary anatomy will be a welcome addition to the literature, and the first glimpse of such analyses (presented here) indicates vastly different carpal kinematics in knuckle-walking chimpanzees compared to fist-walking orangutans.

The contribution of Patel and Wunderlich (2010) to this special issue is an example of the utilization of dynamic biomechanics methods such as kinematic and kinetic analysis to the study of primate locomotion and evolution. These authors demonstrate that habitually terrestrial monkeys adopt a palmigrade hand posture while moving at high speeds, as opposed to the digitigrade hand postures they exhibit at slower speeds. Such a transition in hand postures is attributed to increased ground reaction forces experienced at higher speeds, which are countered by redistributing the forces across more of the hand surface when palmigrade postures are adopted. Thus, this transition in hand postures may represent a selective advantage for preserving fragile hand bones by moderating strain in phalanges and metacarpals, as hands are extremely important organs not only for locomotion, but also for social behavior and feeding.

Ryan and Walker (2010) use high-resolution micro CT to investigate trabecular bone structure in humeral and femoral heads of anthropoid primates using a variety of locomotor repertoires. Their study finds that femoral head trabecular bone volume is significantly higher than trabecular bone volume in the humerus in all taxa, but that humeral trabecular bone is more isotropic than femoral trabecular bone, independent of locomotor behavior.

Finally, the study by Organ (2010) re-examines the functional anatomy of platyrrhine tails using a combination of traditional anthropometric methods and peripheral quantitative CT, a form of CT with resolution intermediate between conventional CT and micro CT. This detailed analysis demonstrates that prehensile tails are comprised of longer proximal tail regions than nonprehensile tails, and that the vertebrae of prehensile tails have better developed muscle attachment sites and are capable of withstanding higher torsional and bending stresses than nonprehensile tails. Furthermore, the disparities between prehensile and nonprehensile tail vertebrae become more evident further distally within the tail sequence. This study also presents strong evidence for the functional convergence of tail structure between two different lineages of platyrrhines with independent evolution of prehensile tails: atelines and Cebus. Taken together, the convergent morphologies associated with prehensile tails make them effective adaptations to navigating arboreal habitats.

CONCLUSIONS

This special issue of The Anatomical Record presents 17 articles using new approaches and many advanced techniques and novel experimental designs to study functional anatomy and biomechanics in primate feeding and locomotor complexes. We hope these articles speak to Kinzey's (1967, p 118) assertion that “…more data are needed particularly on what animals actually do in their various natural habitats in daily activities…also on the anatomy of the joints, their ranges of motion, and the muscles acting upon them. When these data are accumulated and the conclusions derived therefrom tested in experimental situations, we will be in a better position to understand the adaptive value of the various components of primate locomotor [and feeding] behavior and anatomy.” Undoubtedly, we are in a better position now than we ever have been; only time will tell what we can accomplish and learn about our evolutionary past in the future.

Acknowledgements

The authors thank the participants of the 2008 symposium, “An Evolutionary Perspective on Human Anatomy,” and authors who submitted to this special issue, as well as D. Raichlen and K.L. Eaves-Johnson. They also extend a whole-hearted thanks to the numerous reviewers who took time to assure that the manuscripts in this issue are high-quality. Finally, the authors extend their sincerest gratitude to J. Laitman, associate editor of AR, who enthusiastically supported the publication of this special issue from the beginning.