The development of the vermiculate pattern in the brow region of crania from Indian Knoll, Kentucky

A convoluted brow surface consisting of fine ridges, grooves, and depressions, first identified in ancient fossil hominids and termed the vermiculate pattern (VP), is often low in frequency and of moderate rugosity in crania of anatomically modern human populations. Burials at Indian Knoll, Kentucky, constitute an excellent series for study of the development of the VP, since cranial surfaces are usually well preserved, there are hundreds of immature and mature individuals previously assessed for age, and the VP is high in frequency and rugosity. While a surface pattern resembling a miniature VP is found on the supraorbital surface of all newborns, it is not found on any children age 2 or older. This newborn pattern is probably different in structure and origin from the adult VP. The smooth surface characteristic of children shows evidence of changing to the VP in some adolescents, but the fullest development of the VP occurs in adults. The VP continues to develop in rugosity into the fourth decade, especially in males. These observations indicate that the human VP is different in etiology from somewhat similar brow surfaces found sporadically in immature individuals of some species of nonhuman primates. Statements lumping all vermiculate bone surfaces as "fine cancellous bone" are premature. The human VP development shows no apparent relationship to phases of tooth eruption, as postulated for the appearance of areolar surfaces on brow ridges of immature non-human primates.     

The vermiculate surface pattern in brow ridges of Australopithecines and other very ancient hominids

A convoluted surface pattern of fine ridges, pits, and grooves characterized the brow ridges of Australopithecines and other very ancient fossil hominids. This vermiculate configuration terminated rather abruptly just below the fronto-zygomatic suture in Australopithecines. It was resistant to oriented cracking from weathering or fractures, contrasting with the smooth but structurally oriented zygomatic bone adjacent to it. The pattern apparently developed as individuals matured. The vermiculate pattern seems to have been a feature of brow surface in hominids through much of their identifiable history, despite substantial changes in shape and size of the supraorbital region during human evolution. Limitations on the area of vermiculate surface in Australopithecines suggest that the pattern was associated in some yet undetermined manner with overlying soft tissues. This gives evidence on the cause and functional significance of the vermiculate pattern in Neandertal and modern crania. Problems of describing surfaces as “vermiculate” are raised by observation of elaborations of surface relief on two individuals.     

Cortical surface patterns in human and nonhuman primates

An analysis of skulls from several primate species shows that a “worm-track” surface pattern, first identified in the brow region in fossil adult hominids and subsequently in olive baboons, chimpanzees, and macaques, is also present in numerous other species. Fine cancellous bone and its attendant vermiculate surface pattern have been observed in subadult and adult gelada baboons, gibbons, gorillas, and orangutans as well as in modern Homo sapiens and several Plio-Pleistocene fossil hominids. In contemporary primates, fine cancellous bone has been identified not only in the brow region, but also along the zygomatic arch, on the pterygoid plates, on the maxilla, along the temporal line, on the mastoid process, and in the region of inion. Given the widespread distribution of this trait, caution is advised when using it as a diagnostic indicator of the evolutionary or functional significance of craniofacial morphology.     

Structure of bone in the skulls of Neanderthal fossils

Close inspection of surface bone in skulls of Neanderthal man reveals weathering cracks extensive enough in one specimen, La Chapelle-aux-Saints, to allow preliminary analysis of major patterns of orientation and to make inferences about functional relationships of structures. The fine structure of the bone of the brow ridges is very different from the rest of the skull in the two adults examined, having a peculiar vermiculate surface pattern. Weathering cracks do not appear in this region. This indicates that Neanderthal brow ridges are not closely related to normal mechanical forces such as chewing exertion. It may, however, give further support to theories of Neanderthal brow ridges as protection for the eyes. The localized structure of bone often differs from region to region, and offers new possibilities for the analysis of both contemporary and fossil forms.     

Studies on the condition and structure of bone of the Saldanha fossil cranium.

The external surface of the Saldanha cranium shows extensive exfoliation and cracking. In a few places remnants of the probable original bone surfaces can be observed. These are orange-brown in color, contrasting with the nearly white color of exposed deeper layers, and are subdivided into small segments with pits in their centers. Causes of the color differences are uncertain but merit investigation. The surface cracking and exfoliation probably result from weathering before fossilization. This conclusion is based on the observation that the endocranial surfaces show no such effects, despite the scattering of the cranial fragments at the time of discovery. A depressed fracture in the frontal bone indicates a heavy blow at or shortly after the time of death. This blow probably created some of the fragments, but there are also incomplete fracture cracks which may have resulted from the blow. Unresolved taphonomic problems include the manner in which the cranium held together after decay of soft tissues allowed weathering, and the manner in which the fragments were subsequently scattered. Chips from the cranial vault indicate that the outer table was very thick, tending to support recent proposals that the specimen and assoicated fauna and tools are from a considerably earlier time period than originally believed. The surface damage to the brow ridges gives information on the structure of deeper layers. These are lacking orientation, supporting the hypothesis that hominid brow ridges are not primarily a response to masticatory forces, but may afford protection for the eyes.     

A statistical analysis of the literature on sexual dimorphism in primates

The annotated bibliography on sexual dimorphism in primates compiled by the authors was analysed considering the distribution of entries by keytitles, keywords, kind of periodicals and years of publication. A growing interest in this field was observed especially since the 1970s, but a relative scarcity of basic methodological papers was found. Articles on extant human populations and on living nonhuman primates are much more frequent than works on fossil primates and ancient humans.     

Primates in northern Viet Nam: A review of the ecology and conservation status of extant species,with notes on pleistocene localities

We discuss the distribution of living and fossil primates in northern Viet Nam, integrate new localities into the known ranges, and address the ecological parameters and status of extant primate species. In addition, we interpolate fossil specimens from Pleistocene cave sites into the discussion of current ranges. This approach provides a unique glimpse into the past ranges of extant species in a tropical setting, which is unavailable for most regions of the world. Finally, we review the effects of ecocide and other anthropogenic threats to nonhuman primates in Viet Nam.     

Subperiosteal brow lifts without fixation

Most surgeons today advocate an endoscopic subperiosteal brow lift for surgical correction of the upper third of the face. At the author's clinic, this operation has been performed since 1994 and the subgaleal bicoronal brow lift is no longer used. In earlier investigations, the author showed that the subperiosteal approach (n = 60) gives a better result than the subgaleal method (n = 60) when compared 1 year after surgery. In the literature, however, there are no published data regarding the long-term results of subperiosteal brow lifts. The author took material from his earlier investigations and looked at the same patients 5 years postoperatively. He compared the subperiosteal approach (n = 30) with the subgaleal brow lift (n = 15) and found that after 5 years the brows of the subgaleal patients were on the same level as they were before surgery, but in the group of subperiosteal brow lifts, almost all of the brows were higher 5 years after surgery than they were 1 year after surgery, with a mean increase in height of 2.5 mm. These findings led the author to the question whether scalp fixation was necessary at all when performing a subperiosteal brow lift. He performed 20 subperiosteal endoscopic brow lifts where scalp fixation was not used at all, relying only on changing the balance of muscle vectors around the eyebrows. Using a computerized instrument, measurements were made of the distance between the medial canthus and the top of the eyebrow, the midpupil and the top of the eyebrow, and the lateral canthus and the top of the eyebrow. All patients were measured before and 1 year after surgery. The author found an increase of the vertical height from the midpupil to the top of the brow, with an average increase of 3.9 mm. There were no differences between patients who had only a brow lift and those who had a brow lift and an upper blepharoplasty at the same time. The author concludes that for most cases where an increased vertical height of the brows of more than 4 mm is not needed, it is not necessary to use scalp fixation to achieve a natural result.     

Growth layers and incremental markings in hard tissues; a review of the literature and some preliminary observations about enamel structure in Paranthropus boisei

The general factors underlying the formation of growth layers and incremental markings in hard tissues are reviewed with particular reference to fossil hominid tooth enamel. The experimental and circumstantial evidence that point to a slowing of enamel matrix secretion in a daily (circadian) and near weekly (circaseptan) mode during tooth formation is also reviewed. Data from previous studies in which the number of daily increments between adjacent striae of Retzius have been recorded in primates are reviewed and new data are presented for this repeat interval in fossil hominids. The factors likely to influence the number of striae of Retzius beneath the cuspal regions of anterior teeth are outlined and the limitations of employing surface incremental features to obtain estimates for age at death of an individual are also discussed. It is concluded that there is good evidence to support the hypothesis that perikymata are near weekly incremental phenomena with a likely periodicity of 7,8 or 9 days in fossil hominids. It can also be concluded that at present, better estimates for the age at death of an individual during early phases of the growth period can be obtained from studies of perikymata than by any other non-destructive technique.     

Temporal brow lift using botulinum toxin A

The objective of this study was to determine whether brow elevation occurs as a result of paralysis of brow depressors after botulinum toxin A injection. The study's design was a prospective case series with pretreatment and posttreatment outcome evaluation with statistical analysis at a university-based division of facial plastic surgery private clinic. Twenty-two patients of a consecutive sample desiring a cosmetic enhancement underwent injection of botulinum toxin A directed to brow depressors. Injections consisted of 7 to 10 units of botulinum toxin A (Botox, Allergan, Irvine, Calif.) into selected brow depressor muscle (lateral orbicularis oculi) bilaterally. No patients withdrew for adverse effects. All patients were evaluated 2 weeks after treatment. The outcomes were measured by change in brow elevation along vertical axis extending from both midpupil and lateral canthus to the caudal row of brow hairs with eyes at neutral gaze and the head at Frankfort plane. Preintervention and postintervention brow height was measured by the primary clinical investigator. The average brow elevation from the midpupil observed after selected injection of brow depressors with botulinum toxin A was 1.02 mm (p = 0.038). The average brow elevation from the lateral canthus observed after selected injection of brow depressors with botulinum toxin A was 4.83 mm (p<0.0001). Significant temporal brow elevation occurs as the result of paralysis of brow depressors by using botulinum toxin A injection. This procedure may be considered an alternative to surgical brow elevation.     

A comparison between subgaleal and subperiosteal brow lifts

The author has thought for a long time that the endoscopic subperiosteal brow lift has a better long-term result than the bicoronal subgaleal brow lift; therefore, he stopped doing subgaleal bicoronal brow lifts in 1995 in favor of the endoscopic subperiosteal approach. To discover if this impression could be objectively verified, the author undertook a retrospective study of 120 patients who had a brow lift. They were divided into four groups, depending on the type of operation, and were compared with each other by means of a new digitalized analyzing tool. Measurements of the vertical height from the midpupil to the top of the brow, from the medial canthus to the top of the brow, and from the lateral canthus to the top of the brow were made. Preoperative measurements were compared with postoperative measurements taken after 1 year. No significant difference existed between the preoperative and postoperative values in the patients who had a subgaleal brow lift. In the patients who had a subperiosteal brow lift, there was a mean increase of 7 mm in the vertical height of the brow 1 year after the operation.     

Apparent density of the primate calcaneo‐cuboid joint and its association with locomotor mode,foot posture,and the “midtarsal break”

Primates use a range of locomotor modes during which they incorporate various foot postures. Humans are unique compared with other primates in that humans lack a mobile fore‐ and midfoot. Rigidity in the human foot is often attributed to increased propulsive and stability requirements during bipedalism. Conversely, fore‐ and midfoot mobility in nonhuman primates facilitates locomotion in arboreal settings. Here, we evaluated apparent density (AD) in the subchondral bone of human, ape, and monkey calcanei exhibiting different types of foot loading. We used computed tomography osteoabsorptiometry and maximum intensity projection (MIP) maps to visualize AD in subchondral bone at the cuboid articular surface of calcanei. MIPs represent 3D volumes (of subchondral bone) condensed into 2D images by extracting AD maxima from columns of voxels comprising the volumes. False‐color maps are assigned to MIPs by binning pixels in the 2D images according to brightness values. We compared quantities and distributions of AD pixels in the highest bin to test predictions relating AD patterns to habitual locomotor modes and foot posture categories of humans and several nonhuman primates. Nonhuman primates exhibit dorsally positioned high AD concentrations, where maximum compressive loading between the calcaneus and cuboid likely occurs during “midtarsal break” of support. Humans exhibit less widespread areas of high AD, which could reflect reduced fore‐ and midfoot mobility. Analysis of the internal morphology of the tarsus, such as subchondral bone AD, potentially offers new insights for evaluating primate foot function during locomotion. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

On the Other Hand: Statistical Issues in the Assessment and Interpretation of Hand Preference Data in Nonhuman Primates

I describe methodological and statistical issues in the assessment of hand preference in nonhuman primates and discuss them in the context of a recent paper by McGrew and Marchant (1997) in which they conclude that there is no convincing evidence of population-level hand preferences in nonhuman primates. The criteria used by them to evaluate individual and population-level hand preferences are flawed, which results in an oversimplification of findings in nonhuman primates. I further argue that the classification schema used by McGrew and Marchant (1997) to compare hand preference distributions between species is theoretically weak and does not offer a meaningful way to compare human and nonhuman primate handedness.     

Nonhuman primate IgA: genetic heterogeneity and interactions with CD89

Nonhuman primates are extremely valuable animal models for a variety of human diseases. However, it is now becoming evident that these models, although widely used, are still uncharacterized. The major role that nonhuman primate species play in AIDS research as well as in the testing of Ab-based therapeutics requires the full characterization of structure and function of their Ab molecules. IgA is the Ab class mostly involved in protection at mucosal surfaces. By binding to its specific Fc receptor CD89, IgA plays additional and poorly understood roles in immunity. Therefore, Ig heavy alpha (IGHA) constant (C) genes were cloned and sequenced in four different species (rhesus macaques, pig-tailed macaques, baboons, and sooty mangabeys). Sequence analysis confirmed the high degree of intraspecies polymorphism present in nonhuman primates. Individual animals were either homozygous or heterozygous for IGHA genes. Highly variable hinge regions were shared by animals of different geographic origins and were present in different combinations in heterozygous animals. Therefore, it appears that although highly heterogeneous, hinge sequences are present only in limited numbers in various nonhuman primate populations. A macaque recombinant IgA molecule was generated and used to assess its interaction with a recombinant macaque CD89. Macaque CD89 was able to bind its native ligand as well as human IgA1 and IgA2. Presence of Ag enhanced macaque IgA binding and blocking of macaque CD89 N-glycosylation reduced CD89 expression. Together, our results suggest that, despite the presence of IgA polymorphism, nonhuman primates appear suitable for studies that involve the IgA/CD89 system.     

Genetic analysis of Toll/Interleukin-1 Receptor (TIR) domain sequences from rhesus macaque Toll-like receptors (TLRs) 1–10 reveals high homology to human TLR/TIR sequences

Toll-like receptors (TLRs) form a major group of pattern recognition receptors of the innate immune system that sense molecular patterns on microbes. The cytoplasmic Toll/Interleukin-1 Receptor (TIR) signaling domain is instrumental in inducing a signaling cascade upon recognition of specific ligands by TLRs. Because nonhuman primates are used as models of infectious and immune processes, we sought to obtain an increased understanding of nonhuman primate TLRs. We obtained the nucleotide sequences of the TIR domains of rhesus macaque TLRs 1–10 and examined their genetic relationships to TLRs from humans and mice. Alignment of the deduced amino acid sequences revealed macaque-specific changes mostly outside the conserved Box regions of the TLR/TIR domain. Assessment of mutational biases among TLRs from multiple species revealed a strong overall bias towards synonymous substitutions, with a few short regions showing evidence for positive selection outside the Box regions. This first presentation of the TLR/TIR domain sequences from nonhuman primates indicates that although there are species-specific differences, a high level of sequence homology exists in the critical signaling Box regions of macaque, human, and murine TLR/TIR domains. These findings suggest that animal models, including nonhuman primates, will be useful in modeling human TLR pathophysiology and therapy.     

Optimization of a Novel Non-invasive Oral Sampling Technique for Zoonotic Pathogen Surveillance in Nonhuman Primates

Free-ranging nonhuman primates are frequent sources of zoonotic pathogens due to their physiologic similarity and in many tropical regions, close contact with humans. Many high-risk disease transmission interfaces have not been monitored for zoonotic pathogens due to difficulties inherent to invasive sampling of free-ranging wildlife. Non-invasive surveillance of nonhuman primates for pathogens with high potential for spillover into humans is therefore critical for understanding disease ecology of existing zoonotic pathogen burdens and identifying communities where zoonotic diseases are likely to emerge in the future. We developed a non-invasive oral sampling technique using ropes distributed to nonhuman primates to target viruses shed in the oral cavity, which through bite wounds and discarded food, could be transmitted to people. Optimization was performed by testing paired rope and oral swabs from laboratory colony rhesus macaques for rhesus cytomegalovirus (RhCMV) and simian foamy virus (SFV) and implementing the technique with free-ranging terrestrial and arboreal nonhuman primate species in Uganda and Nepal. Both ubiquitous DNA and RNA viruses, RhCMV and SFV, were detected in oral samples collected from ropes distributed to laboratory colony macaques and SFV was detected in free-ranging macaques and olive baboons. Our study describes a technique that can be used for disease surveillance in free-ranging nonhuman primates and, potentially, other wildlife species when invasive sampling techniques may not be feasible.     

Human Disease-Associated Mitochondrial Mutations Fixed in Nonhuman Primates

A number of human disease-associated sequences have been reported in other species, such as rodents, but compensatory changes appear to prevent these deleterious mutations from being expressed. The aim of this work was to compare the mitochondrial DNA of multiple primates to ascertain whether mitochondrial disease-causing sequences in humans are fixed in nonhuman primates. Indeed, 46 sequences related to human pathology were identified in 1 or more of the 12 studied nonhuman primates, the majority of which were associated with late-onset diseases. Most of these sequences can be explained by the presence of secondary compensatory changes that render these mutations phenotypically inert. Nonetheless, and since humans not only are the longest-lived primate but feature the largest brain, one hypothesis is that a gradual optimization of the human mitochondrion occurred in the hominid lineage driven by the need to optimize the aerobic energy metabolism to delay neurodegeneration. Therefore, it is also proposed that some of these disease-associated sequences in nonhuman primates may be linked to the evolution of human longevity and intelligence, indicating a general pattern of selection on longevity in the course of evolution of the human mitochondrion. [Reviewing Editor: Dr. Martin Kreitman]     

Osteoblast-conditioned media influence the expression of E-selectin on bone-derived vascular endothelial cells

Breast cancer cells frequently metastasize to the ends of long bones, ribs and vertebrae, structures which contain a rich microvasculature that is closely juxtaposed to metabolically active trabecular bone surfaces. This study focuses on the effects of osteoblast secretions on the surface presentation of adhesive proteins on skeletal vascular endothelial cells. Vascular endothelial cells were isolated from trabecular bone regions of the long bones of 7-week-old Swiss Webster mice and also from the central marrow cavity where trabecular bone is absent. Both types of endothelial cells were placed in culture for 7 days, then exposed 24 h to conditioned media from MC3T3-E1 osteoblasts. Conditioned medium (CM) from two different stages of osteoblast development were tested: (1) from immature MC3T3-E1 cells cultured for 5-7 days and (2) from mature MC3T3-E1 cells cultured for 28-30 days. The immature osteoblasts were in a stage of rapid proliferation; the mature osteoblasts formed a matrix that mineralized. Following exposure to the conditioned media, the vascular cells were exposed to anti-P-selectin, anti-E-selectin, anti-ICAM-1, and anti-VCAM-1 to detect the corresponding adhesive proteins on their surfaces. Breast cancer cells are known to bind to these adhesive proteins. Of the four proteins evaluated, E-selectin was consistently found on more cell surfaces (approximately 30%) of bone-derived vascular endothelial cells (BVECs) when exposed to the immature CM whereas vascular endothelial cells from marrow (MVECs) did not show this response to either immature CM or mature CM. These studies suggest that the BVEC blood vessels near immature bone cells express more surface adhesive protein that could enhance entrapment and extravasation of breast cancer cells. Once cancer cells have undergone extravasation into marrow adjacent to bone, they could be readily attracted to nearby bone surfaces.