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Posterior maxillary (PM) plane and anterior cranial architecture in primates.

This study tests several hypotheses of integration between the cranial base and face in primates. After reviewing the definition and anatomical basis for the posterior maxillary (PM) plane, which demarcates the back of the midface at its junction with the sphenoid, we demonstrate how the PM plane can be identified accurately on radiographs, and confirm that it maintains a 90 degrees angle relative to the Neutral Horizontal Axis of the orbits in all primates. In addition, we use the PM plane to test Dabelow's (1929) hypothesis that the orbits and anterior cranial base are more highly integrated in anthropoids than in strepsirrhines, and we test the hypothesis that the midline anterior cranial base (planum sphenoideum) and anterior cranial floor (planum sphenoideum plus cribriform plate) in primates are highly correlated with each other relative to the PM plane. The mean angle between the anterior cranial base and the PM plane does not differ significantly from 90 degrees in anthropoids, but differs significantly in strepsirrhines. The anterior cranial base and anterior cranial floor, however, correlate well with each other relative to the PM plane in both suborders of primates, independent of orbital orientation and configuration. The PM plane, anterior cranial base, and anterior cranial floor, therefore, form an integrated structural complex, a "facial block," whose orientation relative to the posterior cranial base influences craniofacial shape among anthropoids in which orbital orientation influences the orientation of the anterior cranial base. One such effect is that increases in cranial base flexion shorten the antero-posterior length of the nasopharynx.

Animals↗

Primate auditory diversity and its influence on hearing performance.

The auditory region contains numerous structures that have proven useful for phylogenetic classification at various taxonomic levels. However, little work has been done in primates relating differences in morphology to variations in hearing performance. This study documents anatomical and physiological distinctions within primates and begins to address the functional and evolutionary consequences of these and other auditory features. The dimensions of the outer ear (pinna) were measured in cadaveric specimens representing nearly every primate family and used to calculate a shape ratio (height/width). It was found that nonanthropoids have a significantly higher ratio than anthropoids, although the actual height was not found to differ. This indicates that most nonanthropoids have ears that are tall and narrow, whereas monkeys and apes are characterized by ears with more equal height and width dimensions. Eardrum area, stapedial footplate area, and ossicular lever arm lengths were measured in dried specimens to calculate an impedance transformer ratio. A distinction was found between anthropoids and strepsirrhines, with the latter group having a transformer ratio indicative of a higher percentage of acoustic energy transmission through the middle ear. Audiogram data were gathered from the literature to analyze hearing sensitivity and it was found that platyrrhines illustrate more low-frequency sensitivity than like-sized lorisoids. The effects of intraspecific variation on the audiogram results were also examined and were found to produce similar results as the analysis using species mean threshold values. Lastly, correlations between morphological and audiogram variables were examined. Several measures of hearing sensitivity were found to be correlated with pinna shape but correlations with middle ear transmission properties were weaker. In addition to using traditional statistical techniques, phylogenetic corrective methods were applied to address the problem of statistical nonindependence of the data and the results of both analyses are compared. These findings are discussed with respect to how sensory adaptations and phylogenetic history may be related to the current radiation of primates.

Adaptation, Physiological↗

Microsmatic primates: reconsidering how and when size matters.

The terms "microsmatic" and "macrosmatic" refer to species with lesser or greater levels, respectively, of olfactory function. Historically, primates are considered microsmats (olfactory sense reduced) with a concomitant increased emphasis on vision. The olfactory bulbs (forebrain centers that receive peripheral olfactory input) are proportionately smaller in primates compared to most other mammals. Similarly, the regions of the nasal cavity that are covered with olfactory epithelium (containing receptor cells) have proportionately less surface area in primates than other mammals. Thus, the generalization that primates are microsmatic is most frequently stated in terms of the proportional rather than absolute size of olfactory structures. Yet the importance of scaling to body size is unclear in regard to the chemical senses such as the olfactory or vomeronasal systems-do chemosensory structures such as olfactory bulbs and olfactory epithelium exhibit the same neural relationship to body mass that is seen for neural tissues that supply innervation to musculature or the skin? Previous studies examining neuronal density, volume, and/or surface area of the olfactory epithelium illustrate that different conclusions may be supported based on the parameter used. Plots of olfactory bulb volume versus body mass that generated for large-scale taxonomic studies or growth studies benefit from body mass (or total brain volume) with a comparative perspective. However, our examination of proportional versus absolute measurements implies that in comparisons within taxa, body size adjustments needlessly distort the data. As a final consideration, another embryonic derivative of the nasal placode, the vomeronasal organ, may warrant consideration regarding a definition of microsomia versus macrosomia.

Animals↗

Accessory optic system of an anthropoid primate, the gibbon (Hylobates concolor): evidence of a direct retinal input to the medial terminal nucleus.

The accessory optic system (AOS) was studied in an anthropoid primate by using anterograde transport of tritiated amino acids and autoradiographic techniques. The course of the accessory optic tract (AOT) and the retinal projection to the terminal nuclei are described in the gibbon and compared to that of other mammals. The AOT consists of a superior fasciculus, which includes both an anterior and a posterior fiber branch. An inferior fasciculus of the AOT is absent. In contrast to previous reports in haplorhine primates, which describe the AOS as consisting of only the dorsal (DTN) and the lateral (LTN) terminal nuclei, we find that in the gibbon, three cellular groups receive a bilateral projection, predominantly from the contralateral retina. According to cytoarchitecture and topographic location, two of these nuclei correspond to the DTN and the LTN. The third cellular group, situated dorsomedial to the substantia nigra, receives a distinct retinal projection and extends rostrocaudally for 2.0 mm in the mesencephalon. This nucleus is homologous to the dorsal division of the medial terminal nucleus (MTN) in other mammals. There was no evidence for a ventral division of the MTN, which in nonprimates is typically situated at the ventromedial base of the cerebral peduncle. Examination of brain morphology in primates suggests that the ventral division of the MTN has been displaced from its phylogenetically stable location in the medial part of the ventral midbrain to a more dorsal position. This shift appears to be a consequence of the overall morphological influences resulting from the relative enlargement of the pons in this region. The demonstration of a direct retinal projection to the MTN in the gibbon, as well as recent reports in other primates, indicates that a complete AOS consisting of three terminal nuclei is a feature common to all mammals.

Animals↗

A view model which accounts for the spatial fields of hippocampal primate spatial view cells and rat place cells.

Hippocampal spatial view cells found in primates respond to a region of visual space being looked at, relatively independently of where the monkey is located. Rat place cells have responses which depend on where the rat is located. We investigate the hypothesis that in both types of animal, hippocampal cells respond to a combination of visual cues in the correct spatial relation to each other. In rats, which have a wide visual field, such a combination might define a place. In primates, including humans, which have a much smaller visual field and a fovea which is directed towards a part of the environment, the same mechanism might lead to spatial view cells. A computational model in which the neurons become organized by learning to respond to a combination of a small number of visual cues spread within an angle of a 30 degrees receptive field resulted in cells with visual properties like those of primate spatial view cells. The same model, but operating with a receptive field of 270 degrees, produced cells with visual properties like those of rat place cells. Thus a common hippocampal mechanism operating with different visual receptive field sizes could account for some of the visual properties of both place cells in rodents and spatial view cells in primates.

Animals↗

Stability, limb coordination and substrate type: the ecorelevance of gait sequence pattern in primates.

The coordination of limb movements during mammalian locomotion has been well documented in the literature. Most mammals use lateral sequence (LS) gaits, in which a forelimb follows an ipsilateral hind limb during the stride cycle. Primates, however, tend to utilize diagonal sequence (DS) gaits, whereby a contralateral forelimb follows a given hind limb during the stride cycle. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a terminal branch niche. Yet to date, there is surprisingly little evidence to support the advantage of DS gaits for negotiating different aspects of the terminal branch environment. Nonetheless, it is apparent that primates possess unique morphologies and a higher than typically recognized degree of flexibility in gait sequence pattern, both of which likely offer advantages for moving upon discontinuous and unstable terminal branches. This paper reviews potential explanations for the use of DS gaits in primates and considers mechanisms by which gait sequence may be altered during different types of arboreal challenges.

Animals↗

Telomere biology and cellular aging in nonhuman primate cells.

To determine how cellular aging is conserved among primates, we analyzed the replicative potential and telomere shortening in skin fibroblasts of anthropoids and prosimians. The average telomere length of the New World primates Ateles geoffroyi (spider monkey) and Saimiri sciureus (squirrel monkey) and the Old World primates Macaca mulatta (rhesus monkey), Pongo pygmaeus (orangutan), and Pan paniscus (pigmy chimpanzee) ranged from 4 to 16 kb. We found that telomere shortening limits the replicative capacity of anthropoid fibroblasts and that the expression of human telomerase produced telomere elongation and the extension of their in vitro life span. In contrast the prosimian Lemur catta (ring-tailed lemur) had both long and short telomeres and telomere shortening did not provide an absolute barrier to immortalization. Following a transient growth arrest a subset of cells showing a reduced number of chromosomes overgrew the cultures without activation of telomerase. Here we show that the presence of continuous TTAGGG repeats at telomeres and rigorous control of replicative aging by telomere shortening appear to be conserved among anthropoid primates but is less effective in prosimian lemurs.

Animals↗

Alu repeats: a source for the genesis of primate microsatellites.

As a result of their abundance, relatively uniform distribution, and high degree of polymorphism, microsatellites and minisatellites have become valuable tools in genetic mapping, forensic identity testing, and population studies. In recent years, a number of microsatellite repeats have been found to be associated with Alu interspersed repeated DNA elements. The association of an Alu element with a microsatellite repeat could result from the integration of an Alu element within a preexisting microsatellite repeat. Alternatively, Alu elements could have a direct role in the origin of microsatellite repeats. Errors introduced during reverse transcription of the primary transcript derived from an Alu "master" gene or the accumulation of random mutations in the middle A-rich regions and oligo(dA)-rich tails of Alu elements after insertion and subsequent expansion and contraction of these sequences could result in the genesis of a microsatellite repeat. We have tested these hypotheses by a direct evolutionary comparison of the sequences of some recent Alu elements that are found only in humans and are absent from nonhuman primates, as well as some older Alu elements that are present at orthologous positions in a number of nonhuman primates. The origin of "young" Alu insertions, absence of sequences that resemble microsatellite repeats at the orthologous loci in chimpanzees, and the gradual expansion of microsatellite repeats in some old Alu repeats at orthologous positions within the genomes of a number of nonhuman primates suggest that Alu elements are a source for the genesis of primate microsatellite repeats.

Animals↗

Sex and context: hormones and primate sexual motivation.

Gonadal hormones regulate the ability to copulate in most mammalian species, but not in primates because copulatory ability has been emancipated from hormonal control. Instead, gonadal hormones primarily influence sexual motivation. This separation of mating ability from hormonally modulated mating interest allows social experience and context to powerfully influence the expression of sexual behavior in nonhuman primates, both developmentally and in adulthood. For example, male rhesus monkeys mount males and females equally as juveniles, but mount females almost exclusively as adults. Having ejaculated with a female better predicted this transition to female mounting partners than did increased pubertal testosterone (T). It is proposed that increased pubertal T stimulates male sexual motivation, increasing the male's probability of sexual experience with females, ultimately producing a sexual preference for females. Eliminating T in adulthood reduces male sexual motivation in both humans and rhesus monkeys, but does not eliminate the capacity to engage in sex. In male rhesus monkeys the effects of reduced androgens on sexual behavior vary with social status and sexual experience. Human sexual behavior also varies with hormonal state, social context, and cultural conventions. Ovarian hormones influence female sexual desire, but the specific sexual behaviors engaged in are affected by perceived pregnancy risk, suggesting that cognition plays an important role in human sexual behavior. How the physical capacity to mate became emancipated from hormonal regulation in primates is not understood. This emancipation, however, increases the importance of motivational systems and results in primate sexual behavior being strongly influenced by social context.

Animals↗

Sexual dimorphism in primate neonatal body mass.

Data were collected on neonatal body mass for 109 primate species. For 23 species with sample sizes of nine or more for each sex, dimorphism (male/female ratio) in neonatal body mass ranged from 0.94 in Galago senegalensis and Aotus trivirgatus to 1.19 in Pongo pygmaeus. Dimorphism in neonatal body mass was positively correlated both with adult body mass and with dimorphism in adult body mass, but the apparent relationship with adult mass was eliminated after controlling for the relationship with adult dimorphism. Comparative studies concerned with neonatal body mass in primates have almost always ignored sexual dimorphism. However, neonatal sexual dimorphism in primates does exist and appears to be of sufficient magnitude to be biologically significant in some species. It may be important to consider the consequences of neonatal dimorphism for a variety of research questions related to maternal investment, life history, postnatal growth, and the relationship between neonatal size and adult female pelvic dimensions, both in extant and in extinct primates.

Animals↗

The rate of CpG mutation in Alu repetitive elements within the p53 tumor suppressor gene in the primate germline.

Cytosine to thymine transition mutations at the CpG dinucleotide are the most common point mutations in cancer and genetic disease. We calculated the in vivo rate of CpG mutation in the primate germline by deriving a primordial consensus sequence for an Alu repetitive element which inserted into intron 6 of the primate p53 gene 35 to 55 million years ago. Comparison of this primordial sequence to the Alu sequence in intron 6 of present-day primates was used to determine the nature and rate of mutations which occurred during evolution. We estimate the half-life of a CpG nucleotide to be 24 to 60 million years, and the rate constant for mutation at this dinucleotide to be 1.2 x 1O(-8) to 2.9 x 1O(-8) years(-1). These results were confirmed by the analysis of a second Alu sequence in intron 10 of the p53 gene. The in vivo mutation rate is at least 1250-fold slower than the in vitro chemical rate of 5-methylcytosine deamination in double-stranded DNA, showing that current estimates of CpG mutation repair have been significantly underestimated. Furthermore, the mutability of the CpG dinucleotide has led to the depletion of this dinucleotide from the vertebrate genome, and calculations in this study suggest that current levels of the CpG dinucleotide in the primate genome are very close to a steady state equilibrium in which the rate of CpG mutation is equal to the rate of CpG formation by random mutation.

Animals↗

The interaction of primate transferrins with receptors on bacteria pathogenic to humans.

The binding of primate transferrins by receptors in the human pathogens Neisseria meningitidis, Moraxella (Branhamella) catarrhalis, and Haemophilus influenzae was assessed and compared with the binding of anti-human transferrin monoclonal antibodies by primate transferrins. In competitive binding assays the three pathogens showed identical specificity for primate transferrins. Only human, gorilla, chimpanzee and orangutan sera were capable of blocking binding of labelled human transferrin. Direct binding assays and affinity isolation of receptor proteins confirmed that chimpanzee transferrin, but not rhesus monkey transferrin, was capable of effectively binding to the bacterial receptors. Five distinct patterns of binding were seen when five anti-human transferrin monoclonal antibodies were reacted with the primate transferrins and these patterns reflected phylogenetic relatedness of these species to humans. A monoclonal antibody which showed transferrin-binding specificity identical to that seen with the bacterial receptors was found to block binding of human transferrin by receptors in the three bacterial species.

Animals↗

Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis.

DNA sequence data from introns, flanking regions, and the eta globin pseudogene region all show a significantly higher rate of nucleotide substitution in the Old World monkey lineage than in the human lineage after the separation of the two lineages, or, in other words, the data support the hominoid rate-slowdown hypothesis. Data from both protein sequences and DNA sequences show that the rate of evolution is significantly higher in the rodent lineage than in the primate lineage. Furthermore, DNA sequences from introns show that the rate of nucleotide substitution is at least two times higher in rodents than in higher primates. The male-to-female ratio of mutation rate is estimated to be between 3 and 6 in higher primates, whereas it is only 2 in mice and rats. These ratios are similar to the corresponding male-to-female ratios of germ cell divisions in higher primates and in rodents, suggesting that errors in DNA replication during germ cell division are the primary source of mutation, or, in other words, mutation is largely DNA replication-dependent. This conclusion provides further support for the generation-time effect hypothesis.

Animals↗

Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence.

A highly resolved primate cladogram based on DNA evidence is congruent with extant and fossil osteological evidence. A provisional primate classification based on this cladogram and the time scale provided by fossils and the model of local molecular clocks has all named taxa represent clades and assigns the same taxonomic rank to those clades of roughly equivalent age. Order Primates divides into Strepsirhini and Haplorhini. Strepsirhines divide into Lemuriformes and Loriformes, whereas haplorhines divide into Tarsiiformes and Anthropoidea. Within Anthropoidea when equivalent ranks are used for divisions within Platyrrhini and Catarrhini, Homininae divides into Hylobatini (common and siamang gibbon) and Hominini, and the latter divides into Pongina for Pongo (orangutans) and Hominina for Gorilla and Homo. Homo itself divides into the subgenera H. (Homo) for humans and H. (Pan) for chimpanzees and bonobos. The differences between this provisional age related phylogenetic classification and current primate taxonomies are discussed.

Animals↗

A comparative study of higher primate foamy viruses, including a new virus from a gorilla.

Few foamy (spuma) retroviruses have been investigated in molecular detail, despite their previous isolation from several mamalian species, including ten neutralization serotypes from various primates. Here, we have studied a new gorilla foamy virus (SFV-Gg) and investigated its functional and phylogenetic relationship to the human (HFV) and other primate foamy viruses, including that recently described in orangutans (SFV-11). Nucleotide sequencing of PCR products obtained from the R/U5 region of the LTR, gag, and pol genes revealed a close relationship between HFV and three chimpanzee isolates (SFV-6, SFV-7, and SFV-cpz). The SFV-Gg, SFV-11, rhesus macaque (SFV-1), and African green monkey (SFV-3) isolates were more divergent. To explore functional relationships, primate foamy virus transactivation of HFV LTR driven beta-galactosidase expression in a newly constructed cell line, BHLL, was investigated. HFV, SFV-6, and SFV-7 potently transactivated HFV LTR driven lacZ gene expression, SFV-Gg induced expression approximately 10-fold less efficiently, and SFV types 1, 2, 3, and 11 did not significantly transactivate the HFV LTR. It was, thus, possible to assay serum neutralizing activity in SFV-infected primates against HFV, SFV-6, and SFV-7 by reduction of beta-galactosidase activity following infection of the indicator cell line. Sera from infected chimpanzees and gorillas neutralized, to varying degrees, each of these three viruses, whereas orangutan sera did not. Our results, based on DNA sequences and functional assays, support the conclusion that HFV is closely related to foamy viruses of chimpanzee origin.

Animals↗

The catecholaminergic innervation of primate prefrontal cortex.

This paper reviews recent studies indicating that the marked expansion and differentiation of the prefrontal cortex in primates is associated with an increase in the complexity of both the regional density and laminar distribution of catecholaminergic afferents. The innervation patterns of these systems in monkey prefrontal cortex appear to accurately predict those in human prefrontal cortex, suggesting that studies in non-human primates may be reasonably used to generate hypotheses about the nature of involvement of these systems in disorders such as schizophrenia. In addition, the distinctive developmental pattern of the dopaminergic innervation of primate prefrontal cortex and the possibility of an intrinsic catecholaminergic innervation of primate prefrontal cortex may reveal new avenues of investigation into the roles of prefrontal catecholamines in both normal and pathological states.

Afferent Pathways↗

Evolution of nuclear gene families in primates. Copy-number variation in the argininosuccinate synthetase (ASS) pseudogene family and the anonymous DNA sequence, D1S1.

Changes in the copy number of nuclear genes provide the raw material for the creation of new gene functions. To better understand the mechanisms for such events, and their physiologic and evolutionary consequences, it is valuable to study a well characterized and closely related group of species such as primates. Fortuitously, most of the powerful molecular techniques and DNA probes developed for research in humans are equally applicable to non-human primates. We review what is known of copy number variation in primates and describe two informative DNA probes: pAS-1, a cDNA probe to the human urea cycle enzyme argininosuccinate synthetase (ASS), and an anonymous DNA probe, D1S1. In addition to the ASS structural locus on human chromosome 9, pAS-1 detects at least 14 dispersed, processed pseudogenes in humans. The number of pseudogene copies appears to be approximately the same in humans, chimpanzees, gorillas, orangutans and baboons; less in marmosets; and least in some rodents. Chimpanzees and gorillas appear to have all of the human pseudogenes though an Xp copy may be missing from gorillas. The Y pseudogene is apparently absent from orangutans and baboons, and, finally, a comparison of humans and chimpanzees revealed that the number of nucleotide substitutions in the Y chromosome pseudogenes is approximately 1 per 100. D1S1 maps to human chromosome 3 but also detects a high homology copy on chromosome 1. Chimpanzees, gorillas and orangutans all appear to have only the chromosome 3 homolog suggesting that this is the ancestral sequence and that the duplication occurred after separation of humans and the great apes. Both the ASS pseudogene family and the D1S1 system provide valuable information on the evolution of nuclear gene families in primates.

Animals↗

Complement component C4 gene intron 9 as a phylogenetic marker for primates: long terminal repeats of the endogenous retrovirus ERV-K(C4) are a molecular clock of evolution.

The complement component C4 genes of Old World primates exhibit a long/short dichotomous size variation, except that chimpanzee and gorilla only contain short C4 genes. In human it has been shown that the long C4 gene is attributed to the integration of an endogenous retrovirus, HERV-K(C4), into intron 9. This 6.36 kilobase retroviral element is absent in short C4 genes. Here it is shown that the homologous endogenous retrovirus, ERV-K(C4), is present precisely at the same position in the long C4 gene of orangutan and African green monkey. Determination of the short C4 gene intron 9 sequences from human, three apes, two Old World monkeys, and a New World monkey allowed the establishment of consistent phylogenetic trees for primates, which favors a chimpanzee-gorilla clade. The 5' long terminal repeats (LTR) and 3' LTR of ERV-K(C4) in long C4 genes of human, orangutan, and African green monkey have similar sequence divergence values of 9.1%-10.5%. These values are more than five-fold higher than the sequence divergence of the homologous intron 9 sequences between the long and short C4 genes in higher primates. The latter is probably a result of homogenization or concerted evolution. We suggest that the 5' LTR and 3' LTR of an endogenous retrovirus can serve as a reliable reference point or a molecular clock for studies of gene duplication and gene evolution. This is because the 5'/3' LTR sequences were identical at the time of retroviral integration and evolved independently of each other afterwards. Our data provides strong evidence for the short C4 gene being the ancestral form in primates, trans-species evolution, and the "slow-down" phenomenon of the sequence divergence in great apes.

Amino Acid Sequence↗