Volume comparisons in the cerebellar complex of primates. I. Ventral pons

Volumes of the ventral pons (VPo) were measured in 82 brains of primates, Scandentia, and Insectivora, and the relative size of the VPo was expressed by size indices. The reference line was through the prosimian average; the mean index of prosimians was set at 1. The taxonomic groups arranged in a sequence of ascending mean VPo indices were: Insectivora (0.04), prosimians (1.00), monkeys (2.55), apes (4.48) and man (9.44). Thus, the VPo of man is more than 9 times larger than that of isoponderous average prosimians, and more than 230 times larger than that of isoponderous "basal' insectivores. The indices may reflect trends and extent of VPo evolution in primate phylogeny.     

Systematics and body size: implications for feeding adaptations in New World monkeys.

The relationship between body size and feeding ecology is well established for primates. It is argued that the evolutionary history of modern New World monkeys and, in particular, the path to attainment of current body size is significant in understanding the similarities and differences between dietary strategies and other ecological parameters of similar-sized monkeys. Current interpretations of New World monkey evolutionary relationships are reviewed. Based on a synthesis of available body weights and the assumption that the earliest New World monkeys weighed close to 1 kg, similar to modern Aotus and Callicebus, predicted patterns of body size change in each lineage are given. Restrictions on directions of body size change in primates are discussed, and it is shown that "Stanley's Rule" offers a good explanation for differing body size ranges in New and Old World anthropoids. Predicted ecological correlates to body size drawn from the mammalian literature are offered and tested using data on New World monkeys, which show some concurrence and several interesting departures from predicted patterns. Sexual dimorphism in body weight of New World monkey species is reviewed, based on the new summary of body weight data given.     

The development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

Baculum length and copulatory behavior in primates

The length of the baculum (os penis) was measured in 74 adult males representing 46 primate species. These data, and a review of previously published measurements, indicate that variation in baculum length among primates is related to taxonomic and behavioral differences. Thus, many New World monkeys have shorter bacula, relative to body weight, than Old World monkeys. The baculum is shorter in colobine monkeys than in cercopithecines. Among the great apes, reduction of the baculum is more pronounced in Pan and Gorilla than in Pongo. Very long bacula are found in some nocturnal prosimians (eg, Lorisidae) and also in Macaca arctoides. A comparison of baculum length relative to body weight was made in 34 species for which detailed information on copulatory behavi or was available. The presence of an elongated baculum was shown to correlate with copulatory patterns involving prolonged intromission and/or the maintenance of intromission during the postejaculatory interval (eg, Galago crassicaudatus, Loris tardigradus, M, arctoides). The evolutionary significance of these observations is discussed and it is suggeted that similar copulatory patterns may occur in species with elongated bacula (eg, Daubentonia, Perodicticus) for which behavioral data are lacking at present. The same hypothesis also applies to an extinct adapid primate which possessed a very large baculum.     

Incisor size and diet revisited: The view from a platyrrhine perspective

Allometric relationships between incisor size and body size were determined for 26 species of New World primates. While previous studies have suggested that the incisors of Old World primates, and anthropoids in general, scale isometrically with body size, the data presented here indicate a negative allometric relationship between incisor size and body size among New World species. This negative allometry was exhibited by platyrrhines when either upper or lower incisor row length was regressed against body weight, and when either least-squares or bivariate principal axis equations were used. When upper incisor length was plotted against skull length, negative allometry could be sustained using both statistical techniques only when the full sample of 26 species was plotted. The choice of variables to represent incisor size and body size, and the choice of a statistical technique to effect the allometric equation, had a more pronounced impact on the location of individual species with regard to lines of best fit. Platyrrhines as a group have smaller incisors relative to body size than do catarrhines, regardless of diet. Among New World primates, small incisors represent a plausible primitive condition; species with relatively large incisors manifest a phyletic change associated with a dietary shift to foods that require increased incisal preparation. The opposite trend characterizes Old World primates. In spite of the taxonomic differences in relative incisor size between platyrrhine and catarrhine primates, inferences about diet derived from an allometric equation for all anthropoids should prove reliable as long as the species with unknown diet does not lie at the upper end of the body size range for platyrrhines or catarrhines.     

Multivariate dental allometry in primates

Disagreement is current over the question of whether relatively large teeth in some large primates are a natural outcome of growth trends instead of an indication of intrinsic differences. A cross-primate survey of dental scaling relative to skull (and inferred body) size is given in this study, using a principal component technique to measure the multivariate growth relation between two sets of data: dental size and cranial size. Cheek teeth are strongly positively allometric in restriced taxonomic groups, especially in cercopithecoids. Conversely, the allometry drops to an almost linear proportional growth relation when variation in diet is controlled.     

Perinatal life history traits in New World monkeys

Gestation length, neonatal and maternal body weight, and neonatal and adult brain weight data were collected for New World monkeys in an attempt to establish typical patterns of perinatal life history. This study attempts to illuminate the most accurate values from the available data, which suggest that gestation length and prenatal growth rate are broadly conserved in relation to maternal size in New World monkeys. Exceptions to the patterns evident in the data point to derivations in life history strategies. In particular, this study suggests that the extended gestation length of callitrichines is a function of minimum viable neonate size and not exclusively energy minimization associated with simultaneous lactation. Cebus is shown to undergo more postnatal brain growth relative to other New World monkeys, but not as much as previously believed. Alouatta is shown to be relatively small brained at birth as well as in adulthood. Saimiri is shown to present the most unusual package of perinatal life history traits, in which precocial neonates are gestated for a relatively long time and at a slightly faster growth rate than is typical for New World monkeys. © 1996 Wiley-Liss, Inc.     

Growth curves of body weight changes in laboratory-bred female African green monkeys (Cercopithecus aethiops)

Nonlinear growth models having three or four parameter family were applied to individual weight data of female African green monkeys for estimating their growth pattern. The body weight was measured continuously from birth to six years of age with five female laboratory-bred monkeys. A total of 95 weight data were collected from each monkey. The average body weight was 330 g with the standard deviation of +/- 15 g at birth, and 2.71 +/- 0.33 kg at four years of age. The body weight of female African green monkeys was judged to reach a plateau after about four years of age. Five growth models (Gompertz, Logistic, Richards, Bertalanffy, Brody) were applied to these weight to age data. The most suitable coefficient of determination between growth data and growth model was obtained by the application of Gompertz equation. Three parameters of Gompertz equation, mature size (A), rate of maturing (K) and inflexion point (e-1 A) were analyzed in relation to age of menarche. Strong correlations between age of menarche and maturing rate, as well as between age of menarche and inflexion point were observed.     

Features of the prosimian wrist joint in relation to hominoid specializations.

The wrist joint of lemuroid and lorisoid prosimians is examined in relation to variations among higher primates, particularly the specializations characteristic of hominoids. The lorisines Nycticebus and Perodicticus share a metrically defined primitive morphopattern with other prosimians and cercopithecine monkeys, showing little convergence on apes in carpal bone and distal radius and ulna shape.     

Neocortical development and social structure in primates

The relationships between the relative size of the neocortex and differences in social structures were examined in prosimians and anthropoids. The relative size of the neocortex (RSN) of a given congeneric group in each superfamily of primates was measured based on the allometric relationships between neocortical volume and brain weight for each superfamily, to control phylogenetic affinity and the effects of brain size. In prosimians, “troop-making” congeneric groups (N=3) revealed a significantly larger RSN than solitary groups (N=6), and there was a significant, positive correlation between RSN and troop size. In the case of anthropoids, polygynous/frugivorous groups (N=5) revealed a significantly larger RSN than monogynous/frugivorous groups (N=8). Furthermore, a significant, positive correlation between RSN and troop size was found for frugivorous congeneric groups of the Ceboidea. These results suggest that neocortical development is associated with differences in social structure among primates.     

Molecular Evolution of Prolactin in Primates

Pituitary prolactin, like growth hormone (GH) and several other protein hormones, shows an episodic pattern of molecular evolution in which sustained bursts of rapid change contrast with long periods of slow evolution. A period of rapid change occurred in the evolution of prolactin in primates, leading to marked sequence differences between human prolactin and that of nonprimate mammals. We have defined this burst more precisely by sequencing the coding regions of prolactin genes for a prosimian, the slow loris (Nycticebus pygmaeus), and a New World monkey, the marmoset (Callithrix jacchus). Slow loris prolactin is very similar in sequence to pig prolactin, so the episode of rapid change occurred during primate evolution, after the separation of lines leading to prosimians and higher primates. Marmoset prolactin is similar in sequence to human prolactin, so the accelerated evolution occurred before divergence of New World monkeys and Old World monkeys/apes. The burst of change was confined largely to coding sequence (nonsynonymous sites) for mature prolactin and is not marked in other components of the gene sequence. This and the observations that (1) there was no apparent loss of function during the episode of rapid evolution, (2) the rate of evolution slowed toward the basal rate after this burst, and (3) the distribution of substitutions in the prolactin molecule is very uneven support the idea that this episode of rapid change was due to positive adaptive selection. In the slow loris and marmoset there is no evidence for duplication of the prolactin gene, and evidence from another New World monkey (Cebus albifrons) and from the chimpanzee and human genome sequences, suggests that this is the general position in primates, contrasting with the situation for GH genes. The chimpanzee prolactin sequence differs from that of human at two residues and comparison of human and chimpanzee prolactin gene sequences suggests that noncoding regions associated with regulating expression may be evolving differently from other noncoding regions.     

The social structure of primates

A comprehensive comparative study of the social structure of primates revealed: There is no social structure which can be considered typical and discriminative for primates. The varying social structures of the extant primate genera cannot be derived from each other: In contrast it seems that the basic, ancestral condition was that of solitary living animals, loosely aggregated. It can be assumed that the development to a gregarious society took place in two entirely different ways. In terms of primate phylogeny this different development can be shown for the prosimians as well as for the old world and new world monkeys as independently occurring processes. One way of behavioral specialization resulted in close pair bonds or in small family groups, whereas the other led to female groups. The presupposition for the forming of a society based on female groups is the close contact between the individuals and in addition to this, a remarkable social tolerance of females to each other. Social specializations which can be considered transitional from the basic condition are frequently found in prosimians. The kinds of social structures of the particular genera are in close relation to their taxonomic positions in the phylogenetic scala. The number of males in larger social groups of primates is substantially irrelevant as the groups are socially most dependent on the females. The protecting males are socially peripheral. The social units of most of the primate species are matrilocal and endure for several generations. In contrast, the social units of the gibbons and of the pongids are patrilocal and are established anew by the females in each generation. Consequently the social unit disintegrates on the death of the male. In all genera studied, male and female individuals present considerable behavioral differences which can be found even in juveniles. Primates are able to discriminate well known and confident individuals from other less confident; they prefer more confident individuals to less confident ones, and less confident to non-confident. As a consequence of this discriminative ability there is a clear preference for near when compared to distant relatives. The complexity of the social relations is brought about by this ability to discriminate combined with the longevity of primates. This is a characteristic and discriminative feature of the primate order. Dominance relations occur in every social group of primates. Linear hierarchies of dominance have been developed only once in prosimians (Lemur) and also once in simians (Cercopithecinae). Therefore, liner hierarchies are not typical for primates.     

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates

Left-sided maternal cradling has been widely reported in human populations. In this paper, I review the evidence of laterality in maternal cradling and infant positional biases in non-human primates. The review revealed some evidence of population-left sided cradling in great apes but little consistency in bias was found among Old and New World monkeys. Very little data have been reported in prosimians. I further describe how asymmetries in either maternal cradling or infant positional biases may explain individual and species differences in hand preference.     

Patterns of sexual dimorphism in body weight among prosimian primates.

Many primatologists believe that there is no sexual dimorphism in body size in prosimian primates. Because this belief is based upon data that came from only a few species and were largely flawed in some aspect of sample quality, I re-examined the extent of sexual dimorphism in body weight, using weights of 791 adult prosimians from 34 taxa recorded over the last 17 years at the Duke University Primate Center. There was no significant sex difference in body weight in 17 species, but males were significantly larger in Nycticebus pygmaeus, Tarsius syrichta, Galago moholi, Galagoides demidovii, Otolemur crassicaudatus and Otolemur garnettii. Moreover, females were significantly larger in Microcebus murinus. Thus, the general lack of sexual dimorphism could be confirmed, notably for lemurs, but prosimians as a group show more variability in sexual size dimorphism than was previously thought. After including previously published data obtained in the wild from 8 additional species, I found significant heterogeneity in the degree of sexual dimorphism at the family level, but only the Indridae and Galagidae were significantly different from each other. Among the prosimian infraorders, the Lorisiformes were significantly more dimorphic than the Lemuriformes. Differences in dimorphism between higher taxonomic groups are discussed in the context of prosimian evolution, concluding that phylogenetic inertia cannot provide a causal explanation for the evolution of sexual dimorphism. The relative monomorphism of most prosimians may be related to allometric constraints and, especially in the Lemuriformes, to selective forces affecting male and female behavioral strategies.     

Epitope expression on primate lymphocyte surface antigens

The cross-reactivity of peripheral blood mononuclear cells from 28 nonhuman primates was investigated with ten kinds of Leu series of monoclonal antibodies specific to human T-, natural killer/killer-, and B-cells. The chimpanzees possessed all ten epitopes examined but the orangutan lacked Leu4 and Leu7 epitopes and the gibbons lacked Leu4, Leu7, and Leu12 epitopes. In addition to the above epitopes, the Old World monkeys lacked Leu1 and Leu10 epitopes. The Leu3a/Leu2a cell ratios varied from 0 to 1.56 among the 12 macaque species and this enabled classification of these species into three groups. In the New World monkeys, Leu2a epitope was absent, whereas Leu11a epitope was detected in several species and Leu3a epitope was found only in the owl monkeys. The prosimians expressed only HLA-DR epitope.     

A volumetric comparison of the vestibular nuclei in primates

The volumes of each of the four vestibular nuclei, superior, lateral, medial and descending, were measured in 80 brains from 2 species of Scandentia, 18 species of prosimians, and 26 species of anthropoids. Size indices were calculated by comparing species-specific points to the nucleus volume-body weight allometry in prosimians, where the average prosimian was set at 1.00. The indices range from 1.78 in Saimiri to 0.48 in Gorilla, and the distributions by families overlap partially or completely. The observed trend in size indices is independent of changes in the neocortex and the ventral pons; average indices are 1.35 in New World monkeys, 1.20 in Old World monkeys, 0.74 in apes, 0.82 in man. Among prosimians, Galago, Galagoides and Tarsius (leaping locomotion) show significantly higher indices than Nycticebus, Loris and Perodicticus (slow movement without leaping). The lateral vestibular nuclear indices in Pongidae and man are extremely low, about half of those of the average prosimians. Correlation coefficients of size indices between the vestibular nuclei and other motor nuclei, such as the cerebellar nuclei, ventral pons and striatum, are analysed. The ratio of the vestibular nuclear volumes to the total brain volumes and the distribution of percentages of each vestibular nuclear volume to the total complex are also obtained.     

Evidence of social learning in black-and-white ruffed lemurs (Varecia variegata)

Although many studies have examined social learning capabilities in apes and monkeys, experiments involving prosimians remain largely absent. We investigated the potential for social learning in black-and-white ruffed lemurs using a two-action foraging task. Eight individuals were divided into two experimental groups and exposed to conspecifics using one of two techniques to access food. Subjects were then given access to the apparatus and their retrieval techniques were recorded and compared. All subjects made their first retrieval using the technique they observed being demonstrated, and there were significant differences between the two groups in their overall response patterns. These results suggest that prosimians are capable of social learning and that additional long-term field studies may reveal the presence of behavioural traditions similar to those found in other primates.     

Osteoarthritis, calcium pyrophosphate deposition disease, and osseous infection in Old World primates.

Uncertainties as to the nature and implications of osteoarthritis and calcium pyrophosphate deposition disease (CPPD) in primates were subject to critical review through examination of 153 prosimians and 1,250 Old World non-prosimian primates. Osteoarthritis, calcium pyrophosphate deposition disease, and infectious arthritis/osteomyelitis were relatively rare phenomena, affecting only 1.7% and 2.5%, respectively, of free-ranging prosimians and other Old World non-prosimian primates. Frequency of infection in Indri and Presbytis appears to reflect a unique susceptibility or exposure. Papio may have a unique predisposition to CPPD. The dichotomy (frequency and joint distribution) between free-ranging and artificially restrained animals suggests caution in interpretation of osteoarthritis or CPPD in non-free-ranging animals.     

Glutathione metabolism in primate lenses: A phylogenetic study of glutathione synthesis and glutathione redox cycle enzyme activities

Lens wet weights, soluble protein, and activities of γ-glutiamylcysteine synthetase, glutathione synthetase, glutathione peroxidase, and glutathione reductase were determined in primate lenses. The primary sources of lenses were middle-aged adult animals. The Primates, from 23 genera, were categorized into six superfamilies: hominoids (five species), Old World monkeys (seven species), New World monkeys (five species), tarsiers (two species), lemurs (six species), and lorisids (three species). Significant differences between various groups or combinations of groups were noted for γ-glutamylcysteine synthetase, glutathione peroxidase, and glutathione reductase activities. Lenticular γ-glutamylcysteine synthetase activity was very low in the Old World simian lenses and highest in the prosimians. Glutathione peroxidase activity was extraordinarily high in lenses of Old World monkeys. Glutathione reductase activity was low in all the prosimians but tenfold higher in hominoid lenses with intermediate values in monkeys of both the Old World and New World. Glutathione synthetase activity was variable, and no clear pattern which might be useful for primate classification was noted. Lenticular activity ratios of glutathione synthetase:γ-glutamylcysteine synthetase were highest in the Old World simians and lowest in the prosimians. These data with emphasis upon Aotus and the tarsiers were examined with regard to phylogenetic relationships. © 1994 Wiley-Liss, Inc.     

Phylogenetic influences on hormone levels across the primate order

Adrenal and gonadal hormone levels were evaluated in representative species from Prosimii, Ceboidea, Cercopithecoidea, and Hominoidea to determine if endocrine activity was influenced by phylogenetic factors. Most small-bodied New World primates had extremely high levels of cortisol, progesterone, and testosterone when compared with Old World primates. In contrast to the high hormone levels and diversity found in Ceboidea, Old World primates showed a more similar pattern of hormone secretion. Thus, this survey supports earlier reports indicating that the callitricids and smaller cebid monkeys have a distinctive hormone profile. Although higher hormone levels tended to be associated with lower body weight, this effect was not evident in all taxa, and there were many notable exceptions. When species differ from their predicted hormone levels based on phylogenetic heritage and body weight (e.g., titi monkeys), we must look for other biological factors that influence endocrine activity. © 1992 Wiley-Liss, Inc.