The primate subarcuate fossa and its relationship to the semicircular canals part II: adult interspecific variation

Studies have reported an empirical link between the size of the semicircular canals and locomotor agility across adult primates. In this paper, we investigate the possibility that this relationship does not follow from the function of the semicircular canals to sense head rotations, but rather reflects spatial constraints imposed by the subarcuate fossa. The latter sits among the three canals and contains the petrosal lobule of the cerebellar paraflocculus, a structure involved in neural processing of locomotion-related eye movements. Hence, it is feasible that agility-related variations of lobule and fossa size affect the arc size of the surrounding semicircular canals. The present study tests such hypothetical correlations by evaluating canal size, fossa size, and agility among extant adult primates. Phylogenetically informed multivariate regression analyses show that, after controlling for body mass, the size of the subarcuate fossa has a significant positive effect on the overall size of the anterior canal and the width of the posterior canal. Multivariate regressions involving the height of the posterior canal and overall size of the lateral canal are not significant. Further bivariate analyses confirm that fossa size is unlikely to play a role in the previously reported link between agility and the size of the posterior and lateral canals. However, fossa size, especially its opening though the arc of the anterior canal, cannot be excluded as a factor that influences the size of the anterior canal more than agility. The findings show that the most reliable functional signals pertaining to locomotion in species that possess a patent subarcuate fossa are likely to come from the lateral canal and are least likely to come from the anterior canal.     

The primate subarcuate fossa and its relationship to the semicircular canals part I: prenatal growth

Studies have reported a functional link between the arc size of the semicircular canals and locomotor agility across adult primates. However, canal size is spatially interlinked with the subarcuate fossa. This fossa can house the petrosal lobule of the paraflocculus, which also plays a role in coordinating head and eye movements. Consequently, it could be that it is the size of the petrosal lobule and fossa that are directly associated with locomotor agility, and not canal arc size. The apparent association of the latter would only follow from the spatial requirement of the canals to accommodate a suitably enlarged subarcuate fossa and petrosal lobule. This study aims to test the ontogenetic basis of this argument by examining high-resolution magnetic resonance images of fetal samples of Homo sapiens, Macaca nemestrina, and Alouatta caraya. Falsifiable null hypotheses examined are (1) that development of the subarcuate fossa is initiated by growth of the petrosal lobule, and (2) that growth of the semicircular canals and of the subarcuate fossa are independent. The findings confirm that the subarcuate fossa forms independently of a petrosal lobule in all three species, thereby falsifying the first hypothesis. Significant correlations were observed between size variables of the semicircular canals and the subarcuate fossa, particularly between the anterior canal and the opening of the fossa. These results falsify the hypothesis that the canals and fossa grow entirely independently. In the human sample, canal growth outpaces fossa growth, possibly because no petrosal lobule is present in humans. In the other two species, the subarcuate fossa simply seems to fill the space made available by canal growth. However, fossa enlargement cannot be excluded as an influence on size increase in the canals. Nevertheless, taken together, the results suggest that canal size is unlikely to be determined primarily by the spatial requirements of the subarcuate fossa and petrosal lobule, rather than by sensory demands reflected in the empirically established link with locomotor agility.     

High-resolution computed tomography for the comparative study of fossil and extant bone

Special methods have been developed to use computed tomography (CT) for 3-dimensional imaging of both fossil and extant bones. Most commercial CT scanners cannot display the internal structure of fossils because the very high density is beyond the upper limits of the normal CT number scale (Hounsfield scale) of the scanners. X-ray projections from CT scans of fossils were modified by scaling the data to provide an expanded CT number scale, allowing the internal structure of highly fossilized objects to be visualized. These images were compared with state-of-the-art, high-resolution CT images of extant bone. Special image reformatting software was used to provide qualitative and quantitative 3-dimensional imaging. The recent rapid advances in CT technology have made this imaging modality the procedure of choice in much of diagnostic radiology. Use of this tool in paleoanthropology has been limited in the past by restricted access to scanners. However, new developments in CT will make this technique available to many researchers in the near future.     

A comparative study of the trabecular bony architecture of the talus in humans, non-human primates, and Australopithecus

This study tested the hypothesis that talar trabecular microarchitecture reflects the loading patterns in the primate ankle joint, to determine whether talar trabecular morphology might be useful for inferring locomotor behavior in fossil hominins. Trabecular microarchitecture was quantified in the anteromedial, anterolateral, posteromedial, and posterolateral quadrants of the talar body in humans and non-human primates using micro-computed tomography. Trabecular bone parameters, including bone volume fraction, trabecular number and thickness, and degree of anisotropy differed between primates, but not in a manner entirely consistent with hypotheses derived from locomotor kinematics. Humans have highly organized trabecular struts across the entirety of the talus, consistent with the compressive loads incurred during bipedal walking. Chimpanzees possess a high bone volume fraction, consisting of plate-like trabecular struts. Orangutan tali are filled with a high number of thin, connected trabeculae, particularly in the anterior portion of the talus. Gorillas and baboons have strikingly similar internal architecture of the talus. Intraspecific analyses revealed no regional differences in trabecular architecture unique to bipedal humans. Of the 22 statistically significant regional differences in the human talus, all can also be found in other primates. Trabecular thickness, number, spacing, and connectivity density had the same regional relationship in the talus of humans, chimpanzees, gorillas, and baboons, suggesting a deeply conserved architecture in the primate talus. Australopithecus tali are human-like in most respects, differing most notably in having more oriented struts in the posteromedial quadrant of the body compared with the posterolateral quadrant. Though this result could mean that australopiths loaded their ankles in a unique manner during bipedal gait, the regional variation in degree of anisotropy was similar in humans, chimpanzees, and gorillas. These results collectively suggest that the microarchitecture of the talus does not simply reflect the loading environment, limiting its utility in reconstructing locomotion in fossil primates.     

The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach

Non-primate mammalian activity cycles are highly variable across and within taxonomic groups. In contrast, the order Primates has historically been recognized as displaying a diurnal-nocturnal dichotomy that mapped, for the most part, onto the taxonomic division between haplorhines and strepsirhines. However, it has become clear over the past two decades that activity cycles in primates are not quite so clear cut. Some primate species--like many large herbivorous mammals, mustelids, microtine rodents, and shrews--exhibit activity both at night and during the day. This activity pattern is often polyphasic or ultradian (several short activity bouts per 24-hour period), in contrast to the generally monophasic pattern (one long bout of activity per 24-hour period) observed in diurnal and nocturnal mammals. Alternatively, it can vary on a seasonal basis, with nocturnal activity exhibited during one season, and diurnal activity during the other season. The term now generally employed to describe the exploitation of both diurnal and nocturnal phases in primates is 'cathemeral'. Cathemerality has been documented in one haplorhine, the owl monkey, Aotus azarai, in the Paraguayan and Argentinian Chaco and in several Malagasy strepsirhines, including Eulemur spp., Hapalemur sp. and Lemur catta. In this paper, we review patterns of day-night activity in primates and other mammals and investigate the potential ecological and physiological bases underlying such 24-hour activity. Secondly, we will consider the role of cathemerality in primate evolution.     

The learning skills of primates: The rhesus macaque in comparative perspective

Twenty-month-old rhesus monkeys were tested in a modified discrimination-reversal paradigm, which was designed to distinguish abstract learning from stimulus-response associational learning. Previous studies indicate that talapoin monkeys learn associationally and great apes via forming abstract concepts. Adult rhesus monkeys are apparently capable of forming simple abstractions, but learn primarily through associational process. The results of this study show the adolescent rhesus monkeys to be associational learners, with their response patterns indicating more complexity than the talapoins but less than the adult rhesus monkeys. The data suggest that rhesus monkeys develop their low-level capacity of abstract learning with maturation.     

A comparative study of leukocyte counts and disease risk in primates

Little is known about how the risk of disease varies across species and its consequences for host defenses, including the immune system. I obtained mean values of basal white blood cells (WBC) from 100 species of primates to quantify disease risk, based on the assumption that higher baseline WBC counts will be found in species that experience greater risk of acquiring infectious disease. These data were used to investigate four hypotheses: disease risk is expected to increase with (1) group size and population density; (2) greater contact with soil-borne pathogens during terrestrial locomotion; (3) a slow life history; and (4) increased mating promiscuity. After controlling for phylogeny, WBC counts increased with female mating promiscuity, as reflected in discrete categories of partner number, relative testes mass, and estrous duration. By comparison, the social, ecological, and life-history hypotheses were unsupported in comparative tests. In terms of confounding variables, some WBC types were associated with body mass or activity period, but these variables could not account for the association with mating promiscuity. Several factors may explain why hypotheses involving social, ecological, and life-history factors went unsupported in these tests, including the role of behavioral counterstrategies to disease, restrictions on female choice of mating partners, and the effect of transmission mode on parasite strategies and host defenses.     

A comparative study of the gut-associated lymphoid tissue of primates and rodents

Previous studies have suggested that the gut-associated lymphoid tissue (GALT) of man is distinct from that of laboratory animals, but it is not clear whether this is due to environmental or true species difference. We have made a comparative study of rats and baboons because, like rats, baboons are herbivorous and relatively unhygienic but they are phylogenetically much more closely related to man. The Peyer's patches of rats, baboons and man are morphologically very similar in all three species but phenotypically those of man and baboons are different to those of rats. Cells with irregular nuclei ("centrocyte-like" cells) surround the mantle zone in all three species. While these cells express surface IgD and IgM in rats, in man and baboons they express surface IgM or IgA. A population of immunoblasts which express cytoplasmic IgA are present in association with the high endothelial venules of rat Peyer's patches. These cells are not present to the same extent in man or baboons. This suggests that the events between the antigenic stimulation of Peyer's patches and the ultimate seeding of the lamina propria with IgA secreting plasma cells may be different in rodents and primates.     

A comparative study of the gut-associated lymphoid tissue of primates and rodents

Virchows Archiv B Cell Pathology - Previous studies have suggested that the gut-associated lymphoid tissue (GALT) of man is distinct from that of laboratory animals, but it is not clear whether...     

Brain expansion and comparative prenatal ontogeny of the non-hominoid primate cranial base

The basicranium is the keystone of the primate skull, and understanding its morphological interdependence on surrounding soft-tissue structures, such as the brain, can reveal important mechanisms of skull development and evolution. In particular, several extensive investigations have shown that, across extant adult primates, the degree of basicranial flexion and petrous orientation are closely linked to increases in brain size relative to cranial base length. The aim of this study was to determine if an equivalent link exists during prenatal life. Specific hypotheses tested included the idea that increases in relative endocranial size (IRE5), relative infratentorial size (RIE), and differential encephalization (IDE) determine the degree of basicranial flexion and coronal petrous reorientation during non-hominoid primate fetal development. Cross-sectional fetal samples of Alouatta caraya (n=17) and Macaca nemestrina (n=24) were imaged using high-resolution magnetic resonance imaging (hrMRI). Cranial base angles (CBA), petrous orientations (IPA), base lengths, and endocranial volumes were measured from the images. Findings for both samples showed retroflexion, or flattening, of the cranial base and coronal petrous reorientation as well as considerable increases in absolute and relative brain sizes. Although significant correlations of both IRE5 and RIE were observed against CBA and IPA, the correlation with CBA was in the opposite direction to that predicted by the hypotheses. Variations of IDE were not significantly correlated with either angle. Correlations of IPA with IRE5 and RIE appeared to support the hypotheses. However, partial coefficients computed for all significant correlations indicated that changes to the fetal non-hominoid primate cranial base were more closely related to increases in body size than the hypothesized influence of relative brain enlargement. These findings were discussed together with those from a previous study of modern human fetuses.     

The sarcoplasmic reticulum: a comparative study

The diversity of cellular membrane structures associated with regulation of intracellular calcium level is described in several different groups of organisms and cells. All the instances reported refer to cellular processes related to movement, in which calcium ion acts as trigger and/or modulator. In addition, a simplified five-stage picture of the underlying view of evolution of these structures is presented. In short: the choice made by nature in using calcium as intracellular messenger was very early in the history of life; all cellular structures devoted to intracellular calcium regulation, from the simplest form of amoeba to the highly sophisticated apparatus of mammalian skeletal muscle, can be linked together in the chain of evolution. Because the evidence is still sparse, any conclusion more positive would be speculative and of little value. Hopefully, in the coming years, with a better understanding of membrane architecture as a whole and its protein components (i.e. calcium channels, calcium-binding proteins), we will be able to test the first segments of this evolutionary hypothesis.     

A comparative study of neonatal skeletal development in Cebus and other primates

Comparisons of hand/wrist radiographs of neonatal Cebus albifrons (n = 14) and Cebus apella (n = 4) with those of Saimiri sciureus boliviensis (n = 9) and Macaca mulatta (n = 63) reveal that the cebid monkeys show much less skeletal ossification at birth than macaques. Differences in gestation time alone cannot account for the differences in skeletal maturity at birth in the two groups of monkeys. The skeletal precocity of the newborn macaques indicates that their ossification either begins earlier in gestation or proceeds at a more rapid rate, or both. This, in turn, raises questions about the timing of organogenesis and gestational comparability in cebid and cercopithecid monkeys. The advanced state of ossification seen in macaques at birth is not typical of other groups of anthropoid primates, including Cebus, Saimiri, Pan and Homo, and may represent an ontogenetic specialization.     

Patterns of astragalar fibular facet orientation in extant and fossil primates and their evolutionary implications

A laterally sloping fibular facet of the astragalus (=talus) has been proposed as one of few osteological synapomorphies of strepsirrhine primates, but the feature has never been comprehensively quantified. We describe a method for calculating fibular facet orientation on digital models of astragali as the angle between the planes of the fibular facet and the lateral tibial facet. We calculated this value in a sample that includes all major extant primate clades, a diversity of Paleogene primates, and nonprimate euarchontans (n = 304). Results show that previous characterization of a divide between extant haplorhines and strepsirrhines is accurate, with little overlap even when individual data points are considered. Fibular facet orientation is conserved in extant strepsirrhines despite major differences in locomotion and body size, while extant anthropoids are more variable (e.g., low values for catarrhines relative to non‐callitrichine platyrrhines). Euprimate outgroups exhibit a mosaic of character states with Cynocephalus having a more obtuse strepsirrhine‐like facet and sampled treeshrews and plesiadapiforms having more acute haplorhine‐like facets. Surprisingly, the earliest species of the adapiform Cantius have steep haplorhine‐like facets as well. We used a Bayesian approach to reconstruct the evolution of fibular facet orientation as a continuous character across a supertree of living and extinct primates. Mean estimates for crown Primatomorpha (97.9°), Primates (99.5°), Haplorhini (98.7°), and Strepsirrhini (108.2°) support the hypothesis that the strepsirrhine condition is derived, while lower values for crown Anthropoidea (92.8°) and Catarrhini (88.9°) are derived in the opposite direction. Am J Phys Anthropol 151:420–447, 2013.© 2013 Wiley Periodicals, Inc.