The ontogeny of cranial sexual dimorphism in two old world monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae)

Allometric and heterochronic approaches to sexual dimorphism have contributed much to our understanding of the evolutionary morphology of the primate skull and dentition. To date, however, extensive studies of sexual dimorphism have been carried out only on the great apes and a few cercopithecine monkeys. To fill this gap, representative dimensions of the skull were collected among ontogenetic series of two dimorphic Old World monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae). The ontogeny of cranial sexual dimorphism was evaluated with least-squares bivariate regression, analysis of covariance (ANCOVA), and analysis of variance (ANOVA). Results indicate that within each species the sexes typically exhibit nonsignificant differences in ANCOVAs of ontogenetic trajectories, except for bivariate comparisons with bicanine breadth. AmongMacaca fascicularis, ANOVAs between males and females of common dental ages show that adult, and frequently subadult, males are significantly larger than females, i.e., sexual dimorphism develops via time and rate hypermorphosis (males primarily grow for a longer time period as well as faster). AmongNasalis larvatus, however, comparisons between males and females of common dental ages indicate that only adult males are significantly larger than females, i.e., sexual dimorphism develops primarily via time hypermorphosis (males grow for a longer time period). Within both species, females appear to exhibit an early growth spurt at dental age 2; that is, many cranial measures for females tend to be larger than those for males. Measures of the circumorbital region (e.g., browridge height), body weight, and bicanine breadth exhibit typically the highest sexual dimorphism ratios. The fact that postcanine toothrow length and neurocranial volume (less so inNasalis) demonstrate very low dimorphism ratios generally supports assertions that postnatal systemic growth (and associated selective pressures thereon) exerts a greater influence on facial, but not neural, dental, or orbital, development (Cochard, 1985, 1987; Shea, 1985a,b, 1986; Shea and Gomez, 1988; Sheaet al., 1990). Additional consideration of ontogenetic differences between species generally supports previous functional interpretations of subfamilial differences in cranial form related to agonistic displays in cercopithecine monkeys (Ravosa, 1990).     

Animal behaviour: old world monkeys build new world order

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

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

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.     

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.     

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.     

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.     

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.     

Chromosome evolution in new world monkeys (platyrrhini)

During the last decades, New World monkey (NWM, Platyrrhini, Anthropoideae) comparative cytogenetics has shed light on many fundamental aspects of genome organisation and evolution in this fascinating, but also highly endangered group of neotropical primates. In this review, we first provide an overview about the evolutionary origin of the inferred ancestral NWM karyotype of 2n = 54 chromosomes and about the lineage-specific chromosome rearrangements resulting in the highly divergent karyotypes of extant NWM species, ranging from 2n = 16 in a titi monkey to 2n = 62 in a woolly monkey. Next, we discuss the available data on the chromosome phylogeny of NWM in the context of recent molecular phylogenetic analyses. In the last part, we highlight some recent research on the molecular mechanisms responsible for the large-scale evolutionary genomic changes in platyrrhine monkeys.     

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.     

Karyotypic fission theory and the evolution of old world monkeys and apes

The karyotypes of living catarrhines are correlated with the current concepts of their fossil record and systematic classification. A phylogeny, beginning at the base of the Oligocene, for those animals and their chromosome numbers is presented. Todd? (1970) theory of karyotypic fissioning is applied to this case — three fissioning events are hypothesized. A late Eocene event (the primary catarrhine fissioning) is hypothesized to underlie the diversification of the infraorder Catarrhini into its extant families, the second fissioning underlies the radiation of the Pongidae/Hominidae in the Miocene and the third accounts for the high chromosome numbers (54–72) and the Neogene (Miocene-Pliocene-Pleistocene) radiation of members of the genus Cercopithecus. Published catarrhine chromosome data, including that for “marked” chromosomes (those with a large achromatic region that is the site for ribosomal RNA genes) are tabulated and analysed. The ancestral X chromosome is always retained in the unfissioned metacentric state. The Pongidae/Hominidae have 15 pairs of mediocentric chromosomes that survived the second fissioning whereas the other chromosomes (besides the X) are thought to be fission-derived acrocentrics. Both the detailed karyology and the trend from low to high numbers is best interpreted to support Todd? concept of adaptive radiations correlated with karyotypic fissioning in ancestral populations.     

Humans and old world monkeys have similar patterns of fetal globin expression

The expression of epsilon- and gamma-globin mRNA and protein has been determined in three Old World monkey species (Macaca mulatta, Macaca nemestrina, and Cercopithecus aethiops). Using RT-PCR with primers for epsilon- and gamma-globin, both mRNAs were detected in early fetal stages, whereas at 128 days (85% of full term), only gamma was expressed. High-performance liquid chromatography was used for separation and quantitation, and matrix-assisted laser desorption/ionization mass spectrometry was used for identification of globin polypeptides. An alpha-globin polymorphism was observed in all of the species examined. During fetal life, gamma-globin was the predominant expressed beta-type globin. The red blood cells of infants still contained substantial amounts of gamma-globin, which declined to negligible levels in 14 weeks as beta-globin expression reached adult values. The ratio of gamma1- to gamma2-globins (equivalent to Ggamma/Agamma in humans) was approximately 2.5, similar to the Ggamma/Agamma ratio observed in humans. Thus, gamma-globin gene expression in these Old World monkeys species has three features in common with human expression: expression of both duplicated gamma genes, the relative preponderance of gamma1 over gamma2 expression, and the delay of the switch from gamma- to beta-globin until the perinatal period. Thus, the catarrhines seem to share a common pattern of developmental switching in the beta-globin gene cluster, which is distinct from the timing of expression in either prosimians or the New World monkeys. Our results indicate that an Old World monkey, such as Rhesus, could serve as a model organism (resembling humans) for experimentally investigating globin gene expression patterns during the embryonic, fetal, and postnatal stages.     

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.     

Hearing and communication in blue monkeys (Cercopithecus mitis)

Hearing and vocal communication in blue monkeys (Cercopithecus mitis) was studied within an ecological context. Field measurements of the acoustical characteristics of the blue monkey's natural habitat were conducted in the Kibale forest (Uganda) and in Kakamega forest (Kenya). Measurements of background noise levels indicated that vocal communication pitched in the 100–1000-Hz frequency band would be relatively unimpeded by disruptive background noises. Furthermore, measurements of the propagation rate of audio signals indicated that calls pitched in the 125–200-Hz region penetrated the forest with minimal decrement in amplitude. Tests of the blue monkey's acoustic sensitivyty and range of hearing were conducted in the laboratory with standard audiometric procedures. Hearing in the blue monkey was characterized by a U-shaped function, with maximum sensitivity of about 5 dB SPL spanning a four-octave range from 1 to 16 kHz. The hearing of blue monkeys was superior to human hearing for tones below 500 Hz and above 8 kHz in frequency. A comparative analysis of primate hearing indicated that the blue monkey was approximately 18 dB more sensitive to low-frequency tones than the comparably sized, semi-terrestrial rhesus monkey (Macaca mulatta). Furthermore, blue monkeys exhibit phonatory specializations for vocal production in this relatively unused, low-frequency band of 125–200 Hz. These specializations for low-frequency vocal production and low-frequency hearing collectively act to increase the effective distance of long-range acoustic communication in the forest canopy.     

The Miocene differentiation of old world Pecora (Mammalia)

Dental and horn core/antler morphology is discussed for some representative lower and middle Miocene pecorans in a review of the phylogeny and early zoogeography of the modern Old World families. Giraffes and bovids are more closely related than either is to deer. Andegameryx, Walangania and Teruelia are related to giraffoids plus bovoids together; Amphimoschus and Hispanomeryx are a probable sister group of bovoids; Propalaeoryx is the sister group of the giraffids plus climacoceratids. Procervulus and Lagomeryx may be closer to modern deer than are Stephanocemas and Dicrocerus but all are included in the Cervidae. The horn structure of Palaeomeryx has resemblances to giraffids, but its teeth and postcranial bones are more like cervids and it is placed in the Cervoidea. Pecorans seem to have evolved in Eurasia and there gave rise to deer. By the early Miocene some pecorans had entered Arabo‐Africa where they gave rise to giraffids and probably bovids. The relationships and zoogeography of the early bovids Eotragus, Homoiodorcas and Caprotragoides are likely to be important for later bovid history.     

The term "lateral recess" and craniofacial pneumatization in old world monkeys (Mammalia, Primates, Cercopithecoidea)

The primate superfamily Cercopithecoidea (or Old World monkeys) is characterized by a widespread lack of the maxillary sinus, a paranasal pneumatic space found in most other eutherian mammals. Previous discussions of the distribution of pneumatization in the group, however, have been ambiguous and contradictory, and have been further complicated by discussion of a poorly defined structure named the "lateral recess," linked implicitly to the maxillary sinus. Computed tomography (CT) was applied to dry crania of all cercopithecoid genera to evaluate the morphological relevance of the term "lateral recess." Results suggest that the "lateral recess" is a structural consequence of changes in skull form unrelated to pneumatization. Thus, the term should be abandoned. All Old World monkeys (except the genus Macaca) are found to lack the maxillary sinus, but a previously undescribed bulla, only separated from the nasal cavity anteriorly, was discovered in the Chinese golden monkey Rhinopithecus. If this bulla is related to the paranasal sinuses, it suggests that the initial change in cercopithecoid cranial evolution was a suppression of pneumatic development, which may have been subsequently reversed twice in the history of the group, in Macaca and Rhinopithecus.