Chromosome phylogenies of man,great apes,and old world monkeys

The karyotypes of man and of the closely related Pongidae — chimpanzee, gorilla, and orangutan — differ by a small number of well known rearrangements, mainly pericentric inversions and one fusion which reduced the chromosome number from 48 in the Pongidae to 46 in man. Dutrillaux et al. (1973, 1975, 1979) reconstructed the chromosomal phylogeny of the entire primate order. More and more distantly related species were compared thus moving backward in evolution to the common ancestors of the Pongidae, of the Cercopithecoidae, the Catarrhini, the Platyrrhini, the Prosimians, and finally the common ancestor of all primates. Descending the pyramid it becomes possible to assign the rearrangements that occurred in each phylum, and the one that led to man in particular.The main conclusions are that this phylogeny is compatible with the occurrence during evolution of simple chromosome rearrangements — inversions, fusions, reciprocal translocation, acquisition or loss of heterochromatin — and that it is entirely consistent with the known primate phylogeny based on physical morphology and molecular evolution. If heterochromatin is not taken into account, man has in common with the other primates practically all of his chromosomal material as determined by chromosome banding. However, it is arranged differently, according to species, on account of chromosome rearrangements. This interpretation has been confirmed by comparative gene mapping, which established that the same chromosome segments, identified by banding, carry the same genes (Finaz et al., 1973; Human Gene Mapping 8, 1985).A remarkable observation made by Dutrillaux is that different primate phyla seem to have adopted different chromosome rearrangements in the course of evolution: inversions for the Pongidae, Robertsonian fusions for the lemurs, etc. This observation may raise many questions, among which is that of an organized evolution. Also, the breakpoints of chromosomal rearrangements observed during evolution, in human chromosomal diseases, and after ionizing irradiation do not seem to be distributed at random.Chromosomal rearrangements observed in evolution are known to be harmful in humans, leading to complete or partial sterility through abnormal offspring in the heterozygous state but not in the homozygous state. They then become a robust reproductive barrier capable of creating new species, far more powerful than gene mutations advocated by neo-Darwinism. The homozygous state may be achieved especially through inbreeding, which must have played a major role during primate evolution. Whether new species derive from unique individuals or couples (Adam and Eve), or through a populational process, remains a matter for discussion.     

New data and a discussion of infant killing in old world monkeys and apes.

Information on infant killing by males in reviewed and extended by personal communications and observations. Most cases of infant killing reported occurred during periods when a new alpha male was establishing himself and during arranged encounters of strangers or unfamiliar individuals in captivity. There seem to be no specific releasing stimuli for infant killing, but rather the lack of familiarity between male and females, their nonacceptance of him in the whole set of roles tied to the alpha status, and his special motivational condition as new alpha lead him to a state, in which attacks on infants may result. Infant killing is considered to have a selection advantage by increasing one's own reproduction success while reducing the one of other males.     

Facial anatomy of Victoriapithecus and its relevance to the ancestral cranial morphology of old world monkeys and apes

Recently discovered Craniofacial fossils of the middle Miocene cercopithecoid Victoriapithecus are described. The frontal, zygomatic, maxilla, and premaxilla anatomy differ from the previously proposed colobine-like ancestral cercopithecoid morphotype in several significant respects. This morphotype was based on the assumption that features held in common by subordinate hominoid and cercopithecoid morphotypes (Colobinae and Hylobatidae) are primitive for Old World monkeys. Cranial similarities between Victoriapithecus, which represents the sister-group of both colobine and cercopithecone monkeys, and the shorter-snouted Cercopithecinae (Macaca and Cercopithecus) indicate that the last common ancestor of Old World monkeys possessed the following features: a narrow interorbital septum, moderately long snout, moderately long and anteriorly tapering premaxilla, large procumbent upper central incisors set anterior to and with longer roots than lateral incisors, moderately tall face below the orbits, teardrop-shaped nasal aperture of low height and moderate width, and probably long and narrow nasal bones. The Victoriapithecus cranium is also characterized by features not present in modern cercopithecids. These include a deep malar region of the zygomatic and the presence of a frontal trigon due to the occurrence of temporal lines that merge with supraorbital costae close to the midline of each orbit and converge anterior to bregma. These features are interpreted as primitive retentions from the basal catarrhine condition as indicated by the occurrence of these features among primitive catarrhines (Aegyptopithecus) and Miocene hominoids (Afropithecus). © 1993 Wiley-Liss, Inc.     

Long bone articular and diaphyseal structure in old world monkeys and apes. I: locomotor effects

The relationship between locomotor behavior and long bone structural proportions is examined in 179 individuals and 13 species of hominoids and cercopithecoids. Articular surface areas, estimated from linear caliper measurements, and diaphyseal section moduli (strengths), determined from CT scans, were obtained for the femur, tibia, humerus, radius, and ulna. Both within-bone (articular to shaft) and between-bone (forelimb to hindlimb) proportions were calculated and compared between taxa. It was hypothesized that: 1) species emphasizing slow, cautious movement and/or more varied limb positioning (i.e., greater joint excursion) would exhibit larger articular to cross-sectional shaft proportions, and 2) species with more forelimb suspensory behavior would have relatively stronger/larger forelimbs, while those with more leaping would have relatively stronger/larger hindlimbs. The results of the analysis generally confirm both hypotheses. Several partial exceptions can be explained on the basis of more detailed structural-functional considerations. Associations between locomotion and structural proportions can be demonstrated both across major groupings (hominoids and cercopithecoids) and between relatively closely related taxa, e.g., mountain and lowland gorillas, siamangs and gibbons, and Trachypithecus and other colobines. Furthermore, structure and function do not always covary with taxonomy. For example, compared to cercopithecoids, mountain gorillas have relatively larger joints, like other hominoids, but do not have relatively stronger forelimbs, unlike other hominoids. This is consistent with a locomotor repertoire emphasizing relatively slow movement but with very little forelimb suspension. Proportions of Proconsul nyanzae, Proconsul heseloni, Morotopithecus bishopi, and Theropithecus oswaldi are compared with modern distributions to illustrate the application of the techniques to fossil taxa.     

Molecular evolution of growth hormone gene family in old world monkeys and hominoids

Growth hormone is a classic molecule in the study of the molecular clock hypothesis as it exhibits a relatively constant rate of evolution in most mammalian orders except primates and artiodactyls, where dramatically enhanced rate of evolution (25–50-fold) has been reported. The rapid evolution of primate growth hormone occurred after the divergence of tarsiers and simians, but before the separation of old world monkeys (OWM) from new world monkeys (NWM). Interestingly, this event of rapid sequence evolution coincided with multiple duplications of the growth hormone gene, suggesting gene duplication as a possible cause of the accelerated sequence evolution. Here we determined 21 different GH-like sequences from four species of OWM and hominoids. Combining with published sequences from OWM and hominoids, our analysis demonstrates that multiple gene duplications and several gene conversion events both occurred in the evolutionary history of this gene family in OWM/hominoids. The episode of recent duplications of CSH-like genes in gibbon is accompanied with rapid sequence evolution likely resulting from relaxation of purifying selection. GHN genes in both hominoids and OWM are under strong purifying selection. In contrast, CSH genes in both lineages are probably not. GHV genes in OWM and hominoids evolved at different evolutionary rates and underwent different selective constraints. Our results disclosed the complex history of the primate growth hormone gene family and raised intriguing questions on the consequences of these evolutionary events.     

Old world monkeys compare to apes in the primate cognition test battery

Understanding the evolution of intelligence rests on comparative analyses of brain sizes as well as the assessment of cognitive skills of different species in relation to potential selective pressures such as environmental conditions and social organization. Because of the strong interest in human cognition, much previous work has focused on the comparison of the cognitive skills of human toddlers to those of our closest living relatives, i.e. apes. Such analyses revealed that apes and children have relatively similar competencies in the physical domain, while human children excel in the socio-cognitive domain; in particular in terms of attention sharing, cooperation, and mental state attribution. To develop a full understanding of the evolutionary dynamics of primate intelligence, however, comparative data for monkeys are needed. We tested 18 Old World monkeys (long-tailed macaques and olive baboons) in the so-called Primate Cognition Test Battery (PCTB) (Herrmann et al. 2007, Science). Surprisingly, our tests revealed largely comparable results between Old World monkeys and the Great apes. Single comparisons showed that chimpanzees performed only better than the macaques in experiments on spatial understanding and tool use, but in none of the socio-cognitive tasks. These results question the clear-cut relationship between cognitive performance and brain size and--prima facie--support the view of an accelerated evolution of social intelligence in humans. One limitation, however, is that the initial experiments were devised to tap into human specific skills in the first place, thus potentially underestimating both true nonhuman primate competencies as well as species differences.     

Allomothering behaviour of new and old world monkeys

The holding or transferring of newborn infants at less than 1 month old by individuals other than the mothers was studied in 24 species of New and Old World monkeys under captive conditions. The observed monkey species could be divided into two types. Group A included eight species of three families where the mothers were tolerant to ‘infant transfer’ and readily retrieved their infants from other individuals, the frequency of infant transfer being high. The infant transfer of this group was termed allomothering behaviour. Group B included 16 species of two families where infant transfer did not occur at all or its frequency was very low and the mothers were possessive of their infants. Once transfer did occur, the infant could not be reclaimed with ease. The relationships between the two groups and taxonomic status, life forms and social types were evaluated in a total of 45 species from the present study and the literature. Correspondences were found with social type and taxonomic status. That is, species of Group A were seen only in the family or one-male type, except for one species, although none of this group appeared in the Cercopithecinae regardless of social types. The significance of infant transfer is discussed in relation to the participants' responses to it and the correlations between the two groups and social types.     

Animal behaviour: old world monkeys build new world order

New experimental evidence shows that policing behaviour by dominant monkeys stabilizes and integrates macaque societies.     

The expression of aggression in old world monkeys

The expression of agonistic behavior in adult and juvenile members of both sexes was studied in groups of from 23 to 93 animals representing Macaca mulatta, M. arctoides, M. nemestrina, M. nigra, and Cercocebus atys. Data were collected using focal animal techniques over a period of 1 year for each group. Adult male biting was notably infrequent in all cases, and adult male participation in agonistic encounters was less frequent than for any other age-sex class, especially in the groups with the highest agonistic rates. Adult male agonistic behavior was often expressed as aggression but seldom involved contact forms of aggression, and biting constituted the smallest proportion of contact aggression for all age-sex classes. Adult males were also seldom the targets of aggression and had the highest rates for shaking of objects and bouncing displays. A tendency for the most severe forms of aggressive expression to be most frequent in those animals least capable of inflicting injury was noted in all groups, along with a tendency for aggression to be directed toward immature animals. Sex differences in aggressive expression and responses to aggression were noted, but the frequency of receipt of aggression was not directly reflected in the wounding noted. Different means to achieve the same consequence, infrequent adult male damaging attacks, are suggested to operate in the several groups studied.     

Model life tables for the larger old world monkeys

Mortality statistics for 25 populations of the larger Old World monkeys (members of the subfamily Cercopithecinae) were evaluated with a competing hazard model of mortality. The best eight of these life tables were combined to generate a standard model life table representative of the mortality patterns of these primates. Two applications of the standard model to smooth, graduate, and compare life tables based on limited and defective data are presented.     

Hearing of old world monkeys (Cercopithecinae)

The characteristics of normal hearing were examined in the laboratory for seven species of Old World monkeys. Operant conditioning procedures, coupled with standard audiometric testing methods, were used to assess thresholds of hearing, frequency range of hearing, and differential sensitivity to auditory intensity and frequency. To produce tonal stimulation, an animal was trained to touch and maintain manual contact with a contact-sensitive key and to report hearing the tone by lifting his hand from the key; this response was followed by food reinforcement. When the reporting response occurred without the auditory signal, the animal was punished by a short suspension from the experiment. Additional contingencies were added to ensure stable and reliable responding, and threshold and differential acuity determinations were then made. Threshold was defined as the stimulus value responded to correctly 50% of the time. The frequency range of hearing of all the cercopithecoids tested extended from 60 to 40,000 Hz, an octave above the upper bound of 20,000 Hz for man but well below the 60–70,000 Hz limit for some prosimians. Absolute sensitivity for tonal stimulation in the most sensitive frequency range (1–8 kHz) was about 2 × 10^?4 microbars, comparable to that of other primates tested, including man. Thus, the Old World monkey appears only slightly less sensitive than man to small changes in intensity and frequency of acoustic stimulation. At 1000 Hz at 60 dB above the threshold of audibility, his limit of resolution is about 5 Hz for frequency and 2 dB for intensity.     

Positional behavior in five sympatric old world monkeys

Observations of positional behavior and habitat use were recorded on focal individuals of five species of Old World monkeys at Kibale Forest, Uganda, through the dry season of 1990 and 1991. Cercopithecus ascanius, Cercopithecus mitis, Cercocebus albigena, Colobus badius, and Colobus guereza commonly utilize five similar types of positional behavior (i.e., quadrupedalism, leaping, climbing, sitting, and standing), but in varying frequencies and situations. As a group, colobines use oblique supports and leap more often, and cover greater linear distances during leaps than do cercopithecines. Colobines also prefer to sit (about 90% of all postures), while cercopithecines stand more frequently. Body size differences between the sexes of a species are not reflected in positional behavior. The two small-bodied species climb more and leap less often than the three larger species, which is the reverse of what we would expect. Leaping is the most common method of crossing open spaces within the canopy; but most spatial gaps and leaps are over short distances, usually one meter or less. All five species, regardless of body size or the availability of forest supports, prefer mediumsized supports. Incorporating our work from Uganda with previous investigations of positional behavior reveals few consistent trends with respect to body size or habitat use across primates. © 1995 Wiley-Liss, Inc.     

Jaw morphology and function in living and fossil old world monkeys

This allometric investigation on a sample of 29 cercopithecine and 22 colobine taxa augments the data and implications of prior work on subfamilial variation in mandibular form and function in recent Cercopithecidae. To increase the size range encompassed by living cercopithecines and colobines, I included many of the larger-bodied fossil specimens. These analyses serve to fill a gap in our understanding of size-related changes in masticatory function and symphyseal morphology and curvature in extant and extinct Old World monkeys. Results of subfamilial scaling comparisons indicate that for a given jaw length, colobines possess significantly more robust corpora and symphyses than those of cercopithecines, especially at smaller sizes. Following from previous work, the most plausible explanation for why the subfamilies differ in relative corporeal and symphyseal dimensions is that colobine mandibles experience elevated loads and greater repetitive loading during mastication due, on average, to processing a diet of tough leaves and/or seeds. Although colobines have relatively larger symphyses, subfamilial analyses of symphyseal curvature demonstrate that they evince less symphyseal curvature vis-à-vis cercopithecines of a common size. Moreover, both subfamilies exhibit similar allometric changes in the degree of curvature, such that larger-bodied Old World monkeys have more curved symphyses than those of smaller taxa. Subfamilial scaling analyses also indicate that colobines possess a shorter M2 bite-point length relative to masseter lever-arm length, but not versus temporalis lever-arm length. Thus, as compared to cercopithecines, colobines can recruit less masseter-muscle force to produce similar bite forces during mastication. In both clades, M² bite-point length scales with positive allometry relative to masseter lever-arm length, such that larger species are less efficient at generating molar bite forces. This seems especially important due to the lack of subfamily difference in M² bite-point:temporalis lever-arm scaling (which is isometric across cercopithecids). A consideration of extinct cercopithecids indicates that many of the large-bodied papionins have more robust corpora, due perhaps to a diet which was of similar toughness to that of extant and extinct colobines. However, the biomechanical arrangements of the masseter and temporalis in all but one fossil cercopithecine and all of the fossil colobine specimens are much as predicted for a subfamilial member of its skull size. That most large-bodied papionins with tougher diets nonetheless maintain a less efficient jaw-muscle configuration may be due to stronger offsetting selection for increased relative canine size and gape.     

A biomechanical analysis of mandibular scaling in old world monkeys

Scaling of mandibular dimensions in male Old World monkeys was investigated. Mandibular condyle length, width, and area were regressed separately against body mass and mandibular length for a total of 14 species of Cercopithecoids. Scaling of mandibular depth and width against both body mass and mandibular length were also investigated. When results of regression analysis using the two different independent variables (body mass and mandibular length) were compared, there were significant pattern differences in scaling of cercopithecines versus colobines. Compared to body mass, male cercopithecines had relatively large mandibles (length, width, and depth) and also relatively large condyles (length, width, and area). However, compared to mandibular length, cercopithecines had relatively transversely thin and shallow mandibles and relatively narrow condyles. It is shown that a “biomechanical” interpretation of mandibular scaling patterns against body mass in Old World monkeys demonstrates only that cercopithecines have prognathic faces, an already well-known and well-documented condition. When the biomechanical effects of prognathic faces are controlled for (by scaling against mandibular length), it is shown that cercopithecines possess special adaptations in condyle length while colobines possess special adaptations in condyle width and mandibular depth and width. These results clearly demonstrate the importance of selecting a relevant reference variable in scaling studies where biomechanical interpretations are attempted.     

Mitochondrial cytochrome b gene sequences of old world monkeys: With special reference on evolution of Asian colobines

The classification and phylogenetic relationships of the Old World monkeys are still controversial. For Asian colobines, from three to nine genera were recognized by different primatologists. In the present study, we have sequenced a 424 bp mitochondrial tRNA^Thr gene and cytochrome b gene fragment fromMacaca mulatta, Mandrillus sphinx, Mandrillus leucophaeus, Semnopithecus entellus, Trachypithecus vetulus, T. johnii, T. phayrei, T. francoisi, Pygathrix nemaeus, Rhinopithecus roxellanae, R. bieti, R. avunculus, Nasalis larvatus, andColobus polykomos in order to gain independent information on the classification and phylogenetic relationships of those species. Phylogenetic trees were constructed with parsimony analysis by weighting transversions 5 or 10 fold greater than transitions. Our results support the following conclusions: (1) the Old World monkeys are divided into two subfamilies; (2) that among the colobines,Colobus, the African group, diverged first, andNasalis andRhinopithecus form a sister clade toPygathrix; (3) that there are two clades within leaf monkeys, i.e. 1)S. entellus, T. johnii, andT. vetulus, and 2)T. phayrei andT. francoisi; (4) thatRhinopithecus avunculus, R. roxellanae, andR. bieti are closely related to each other, and they should be placed into the same subgenus; (5) thatRhinopithecus is a distinct genus; and (6) that the ancestors of Asian colobines migrated from Africa to Asia during the late Pliocene or early Pleistocene.