The skin of primates. XLIV. Numerical taxonomy of primate skin

Data on 84 characteristics of the skin of 36 species of primates were extracted from a series of articles describing the histological and histochemical properties of the skin of primates. The data were subjected to a cluster analysis. The results were in reasonably good agreement with orthodox primate taxonomies although some exceptions were apparent. The species clustered into four main groups approximately comparable to Prosimii, Cercopithecoidea, Ceboidea, and Hominoidea. The internal arrangements of the Prosimii, Cercopithecoidea, and Hominoidea are commensurate with standard taxonomic practice. Within the Ceboidea, however, the Atelinae and Alouattinae tend to group with the Hominoidea, Aotus and Saimiri show variable placements, and Callimico groups with the Callithricidae.     

The taxonomic and functional significance of overall body proportions in Primates

Univariate and multivariate study of 22 dimensions describing overall body proportions in 34 primate genera, has shown that these quantities effect a separation between the principal taxonomic divisions of the Primates: Prosimii, Ceboidea, Cercopithecoidea and Hominoidea. The last three do not, however, link to form a single unit, and the separation between the Ceboidea and Cercopithecoidea is imperfect. Some grouping within these major divisions appears, in certain aspects, to be of functional (locomotor), rather than of purely taxonomic, significance. For instance, within the Prosimii, the genera Microcebus, Galago and Tarsius (the two latter being saltatory forms, while leaping is a component of the locomotor pattern of the first) are associated, while within the apes, the Asiatic forms Hylobates, Symphalangus and Pongo (all brachiators) tend to be grouped, as also do the African forms Pan and Gorilla (both, to a large extent, secondarily terrestrial in habit).
The measures especially prominent in effecting this pattern of discrimination are: relative foot length, relative lower limb length and length of foot relative to lower limb length.
Similar, if less clearly defined results emerge if groups of dimensions relating to individual body regions (forelimb, hindlimb, head and trunk) are analysed separately.
The apparent failure of compounds of the measures of the limbs to give an anticipated close reflection of locomotor function stems possibly from the fact that the available dimensions are of an overall nature rather than a reflection of specific biomechanical functions. Such sub-division, according with locomotor pattern as seems to emerge from this study, appears, in fact, to be little more than that implied in current taxonomic schemata.     

Sexual dimorphism and allometry in primate ossa coxae

Five measurements were taken on the ossa coxae of 454 adult primates representing Ceboidea, Cercopithecoidea and Hominoidea. Sex differences in these variables and their relationships to overall body size and sexual dimorphism were tested by means of Student's t-test and regression analysis. The study attempts to clarify the nature of primate pelvic sexual dimorphism, including allometric effects, and more specifically, test the assertion made by Mobb and Wood (1977) that sexual dimorphism in body size in not an important determinant in pelvic sex differences. Variables that contribute to the size of the birth canal tend to be larger in females than males in all taxa studied except two. In these, Hylobates and Alouatta, there were no significant differences between the sexes for any of the five variables. In general, sexual dimorphism in variables contributing to the size of the birth canal was correlated (r ? 0.8) with sexual dimorphism in body size. Furthermore, the coefficients of allometry underlying pelvic sex differences were shown to be moderately correlated (r ? 0.5) with sexual dimorphism in size. The influence of other adaptive factors on primate pelvic sexual dimorphism are also briefly discussed.     

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.     

Deciphering primate phylogeny from macromolecular specificities

A problem in deciphering primate phylogeny, morphological convergence between different evolutionary lines, can be overcome by species comparisons of proteins, macromolecules with specificities closely linked to the genetic code in DNA. Various chemical, electrophoretic, and immunological data on serum and tissue proteins in primates are reviewed with respect to their phylogenetic significance. Much of this data deals with protein specificities in the Hominoidea and depicts a particularly close genetic relationship between man and the African apes. Hominoidea, Cercopithecoidea, Ceboidea, and Lorisoidea are characterized by their proteins as monophyletic or natural taxa, even though the conventional subdivisions within several of these superfamilies are not in complete accord with the protein analyses. The protein evidence supports the conventional grouping of Cercopithecoidea with Hominoidea in the infraorder Catarrhini and the grouping of Catarrhini and Platyrrhini (Ceboidea) in the suborder Anthropoidea. Lemuroidea and Lorisoidea appear to be closer to one another than to either Tupaioidea or Anthropoidea and closer to the Anthropoidea than to the Tupaioidea. Comparisons of primate DNA's by Hoyer and coworkers are demonstrating genetic affinities among primates which agree with those deduced from the comparison of protein specificities. Species differences and similarities in the relative amounts of different protein macromolecules reflect the grade relationships of primates, but, unlike the comparisons of amino-acid sequences or antigenic specificities, are not reliable indicators of phyletic affinities. Data on the ratios of M(uscle) to H(eart) type lactate dehydrogenase in a series of primate brains provides a biochemical example of the concept that there are “lower” (primitive) and “higher” (advanced) grades of evolutionary development among the extant primates.     

Allometric scaling and locomotor function in the primate pelvis

Identification of positional behavior adaptation in the pelvis of primates is complicated by possible confounding effects of body size and phylogeny. Previous work on primate pelvic allometry has focused primarily on sexual dimorphism and its relationship to obstetric constraints in species with large fetal size relative to maternal size. This study investigates patterns of pelvic scaling with a specific aim to understand how pelvic scaling relates to locomotor function. Patterns of scaling of nine pelvic dimensions were examined in a broad comparative sample of 40 species of primates, covering both haplorhines and strepsirrhines, while accounting for phylogenetic nonindependence. Phylogenetic reduced major axis regressions on pelvic scaling patterns suggest that primate-wide patterns are reflected in haplorhine- and strepsirrhine-specific analyses. Many measures scale isometrically with pelvis size, but notably, features of the ilium tend to scale allometrically. As predicted, ilium width and lower ilium cross-sectional area scale with positive allometry, while lower iliac height scales with negative allometry. Further regression analyses by locomotor group suggest that these ilium measures, as well as pubic symphysis and ischium lengths, differ in their scaling patterns according to locomotor mode. These results suggest that scaling differences within primates, when present, are related to functional differences in locomotor behavior and mechanics. This study supports recent work that identifies adaptations to locomotor loading in the ilium and highlights the need for a better understanding of the relationship between pelvic structural mechanics and the mechanical requirements of primate locomotion. Am J Phys Anthropol 156:511–530, 2015. © 2015 Wiley Periodicals, Inc.     

Sexual Dimorphism in the Pelvis of <Emphasis Type="Italic">Microcebus</Emphasis>

Pelvic sexual dimorphism occurs in many anthropoid species and is often attributed to obstetric selection on female pelvic morphology. Few studies of pelvic dimorphism have included strepsirrhine taxa, which typically have relatively smaller infants than those of anthropoids. Because smaller female primates give birth to relatively larger infants, it is possible that the pelves of Microcebus, the smallest extant primate genus, will show some evidence of selection on obstetric adequacy. A comparison of adult female and neonatal body masses indicates that individual neonatal Microcebus are relatively large compared to adult female body mass, even though members of the taxon frequently produce twins. I examined variation in the bony pelvis within a sample of Microcebus. I measured specimens from a single locality, which probably represent 1 population. I measured 8 pelvic and 3 femoral variables to investigate skeletal size and pelvic size and shape dimorphism. Females significantly exceed males in absolute values of sacral width, pelvic height, pubic length, and distances from the pubic symphysis to the ischial tuberosity and points on the sacrum. Measurements of the femur are not significantly greater in females, suggesting that the pelvic differences are not due to skeletal size dimorphism. Significant pelvic shape or ratio differences, calculated via the geometric mean of 5 variables as the denominator, included greater relative pubic length and sacral width in females. Hence selection for obstetric adequacy may occur in the extremely small-bodied Microcebus.     

Immunoglobulin allotypes (Gm,Am, and Km) in non-human primates

The immunoglobulin (Ig) allotypes (Gm, Am, and Km systems) are the genetic markers of the human IgG1, IgG2, IgG3(Gm), IgA2(Am), and kappa light chain(Km). The Gm system, with 18 allotypes shows the greatest degree of polymorphism and we define two Am and three Km allotypes. In this review, we report all the results observed in non-human primates belonging to Hominoidea, Cercopithecoidea, Ceboidea, Lorisoidea, Lemuroidea, and Tupaoidea superfamilies (72 species and subspecies). They concern published data and new unpublished ones. The distribution of the human allotypes and their localization are reported, as well as discordant results observed in some cases with anti-allotype reagents of the same specificity (human and animal origin). Some allotypes are restricted to man. Hominoidea have the greatest number of Gm allotypes and the richest polymorphism. Relatively few allotypes have been found in Cercopithecoidea and Prosimians; most Platyrrhinian species have no allotype. The epitopic polymorphism has been interpreted in terms of evolution of Ig allotypes from primate to man and of the phylogenetic relationships of non-human primate species.     

Evolvability of the Primate Pelvic Girdle

The ilium and ischiopubic bones of the pelvis arise from different regulatory pathways, and as a result, they may be modular in their organization such that features on one bone may be morphologically integrated with each other, but not with features on the other pelvic bone. Modularity at this gross level of organization can act to increase the ability of these structures to respond to selection pressures (i.e., their evolvability). Furthermore, recent work has suggested that the evolution of the human pelvis was facilitated by low levels of integration and high levels of evolvability relative to other African apes. However, the extent of morphological integration and modularity of the bones of the pelvic girdle is not well understood, especially across the entire order of primates. Therefore, the hypothesis that the ilium and ischiopubis constitute separate modules was tested using three-dimensional landmark data that were collected from 752 pelves from 35 primate species. In addition, the hypothesis that the human pelvis demonstrates greatest evolvability was tested by comparing it to all other primates. The results demonstrate that regardless of phylogeny and locomotor function, the primate pelvis as a whole is characterized by low levels of overall integration and high levels of evolvability. In addition, the results support the developmental hypothesis of separate ilium and ischiopubis modular units. Finally, all primates, including humans, apparently share a common pattern of integration, modularity, and evolvability in the pelvis.     

Evolution of femur and tibia in higher primates: Adaptive morphological patterns and phylogenetic diversity

Seventy six metrical traits measured on the femur and tibia of three higher primate groups —Ceboidea, Cercopithecoidea, Hominoidea have been processed by various univariate and multivariate statistical methods to survey the process of evolution of the morphology of the femur and tibia in higher primates. Intragroup and intergroup variability, similarity and differences as well as various aspects of scaling and sexual dimorphism have been analyzed to study adaptive trends and phylogenetic diversity in higher primates, in individual superfamilies and to explore the adaptive morphological pattern of early hominids and basic differences between hominids and pongids. Two basic morphotypes of the femur and tibia in higher primates have been determined. They are (1) advanced hominoid morphotype (hominids and pongids) and (2) ancestral higher primate morphotype (platyrrhine and cattarrhine monkeys, early hominoids, and hylobatids). Cebid lower limb bones are adapted to arboreal quadrupedalism with antipronograde features while femur and tibia of cercopithecid monkeys are basically adapted to the semi-arboreal locomotion. Early hominoids (Proconsul) and hylobatids are morphologically different from pongids; some features are close toAteles or other monkey species. Pongids and hominids are taken as one major morphological group with different scaling and some functional and morphological similarities. Numerous analogous features were described on the lower limb skeleton ofPan andPongo showing analogous ecological parameters in their evolution. Major morphological and biomechanical trends are analyzed. It is argued that early advanced hominoid morphology is ancestral both to the pongids and to early hominids. The progressive morphological trend in early hominids has been found fromA. afarensis with ancestral hominid morphology, toH. habilis with an elongated femur and structural features similar to advanced hominids. A detailed phylogenetic analysis of higher primate femur and tibia is also presented.     

Glutamic-pyruvic transaminase (GPT) in non-human primates,I. Its activities and electrophoretic variation in red blood cells

Glutamic-pyruvic transaminase (GPT) in red cells of 25 species of non-human primates was investigated. There were significant differences in red cell GPT activities among species. Some species in the Prosimiae and the Ceboidea have high red cell GPT activities, while the others of these families examined have low activities. In contrast, red cell GPT activities were too low to be detected in the Cercopithecoidea and the Pongidea. The intraspecific variation of GPT zymograms was observed in Aotes trivirgatus by starch gel electrophoresis.     

Origins of the Ceboidea viewed from an immunological perspective

Ceboid origins were reviewed from the standpoint of immunodiffusion systematics. Computer processing of spur size data from several thousand trefoil Ouchterlony plate comparisons using rabbit antisera to proteins of various primate, tree shrew and elephant shrew species depicted antigenic distances among the various species. A least squares procedure (executed by a new computer program AJUST) corrected for nonreciprocity in the raw antigenic distance matrix. Another computer program (UWPGM) then produced a cladogram from the normalized antigenic distance matrix. Within the cladogram, tree shrews are closer to undisputed primates than to non-primates. The undisputed primates appear as a monophyletic assemblage, consisting of two major lineages: the Strepsirhini, including lorisoid and lemuroid branches, and the Haplorhini. Haplorhini divides into a tarsioid branch and Anthropoidea. The latter consists of two sister groups, Catarrhini (Hominoidea and Cercopithecoidea) and Platyrrhini (Ceboidea). Thus, this cladogram supports those hypotheses of ceboid origins which depict the phyletic line ancestral to the extant Anthropoidea as first separating from strepsirhine and tarsioid lineages before splitting apart into Platyrrhini and Catarrhini. Present evidence does not reveal if the most recent common ancestor of platyrrhines and catarrhines was morphologically still a prosimian or if it existed late enough in the Tertiary to have reached the simian grade.     

Ischial tuberosities and ischial callosities

Ischial callosities are specialised regions of skin and subdermal tissue in the form of fibro-fatty cushions with a tough, non-slip surface, firmly bound to the underlying ischial tuberosity. They occur in primates of the families Cercopithecidae and Hylobatidae. Ischial callosity usage helps animals to adopt stable sitting postures on the tops of branches, particularly during feeding, resting and sleeping. Callosity-like areas in pongids are mainly epidermal specialisations and differ in their development and usage from true callosities. They are similar to the para-callosity skin regions in some ground living cercopithecids. The ischial tuberosity in animals with true callosities has a flat surface which flares out from the lower end of the ischial body and which is devoid of muscle attachments. In animals without callosities the ischial tuberosity is not flared, has a curved surface, and acts as a site for muscle attachment. The ischial tuberosity is relatively broader in animals with callosities than in animals without callosities, although the absolute size of the specimens concerned must be taken into account. The combination of qualitative and quantitative features of fossil ischial tuberosities enables the presence or absence of callosities in these forms to be deduced. The recognition of these features in fossil material might be of use in the elucidation of the evolution of one type of primate arboreal adaptation.     

Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences

The suborder Anthropoidea of the primates has traditionally been divided in three superfamilies: the Hominoidea (apes and humans) and the Cercopithecoidea (Old World monkeys), together comprising the infraorder Catarrhini, and the Ceboidea (New World monkeys) belonging to the infraorder Platyrrhini.We have sequenced an approximately 390-base-pair part of the mitochondrial 12S rRNA gene for 26 species of the major groups of African monkeys and apes and constructed an extensive phylogeny based upon DNA evidence. Not only is this phylogeny of great importance in classification of African guenons, but it also suggests rearrangements in traditional monkey taxonomy and evolution. Baboons and mandrills were found to be not directly related, while we could confirm that the known four superspecies of mangabeys do not form a monophyletic group, but should be separated into two genera, one clustering with baboons and the other with mandrills. Patas monkeys are clearly related to members of the genus Cercopithecus despite their divergence in build and habitat, while the talapoin falls outside the Cercopithecus clade (including the patas monkey). Correspondence to: A.C. van der Kuyl     

Ontogeny and evolution of pelvic diameters in anthropoid primates and in Australopithecus afarensis (AL 288-1)

Pelvic diameters (both anteroposterior [AP] and transverse [TR]) were investigated in a series of anthropoid primates. The ratio of diameters (AP/TR) in each of three pelvic planes (inlet, midpelvis, and outlet) was calculated. In addition to the above, the length of the iliac, pubic, and ischial axes and the angles between these axes were determined. The AP/TR ratio at the pelvic inlet is (reported in millimeters, +/- SD, unless otherwise specified) 1.81 +/- 0.27 in New World monkeys (Cebidae) and Macaca mulatta; 1.53 +/- 0.17 in hylobatids and pongids; 0.87 +/- 0.08 in Homo sapiens; and 0.58 in Australopithecus afarensis (AL 288-1). The AP/TR ratio in the midpelvis is 1.61 +/- 0.23 in nonhominid primates (Cebidae, M. mulatta, hylobatids, and pongids), 1.12 +/- 0.11 in humans, and 0.59 in AL 288-1. In monkeys (Cebidae and M. mulatta), hylobatids, pongids, H. sapiens, and AL 288-1, the ratios of the length of the pubic axis over the ischial axis were 0.84 +/- 0.06, 0.95 +/- 0.07, 1.10 +/- 0.15, and 1.46, respectively; the pubis-ilium angles were 96 +/- 11, 120 +/- 10, 131 +/- 11, and 147 degrees, respectively; and the ischium-pubis angles were 106 +/- 11, 86 +/- 8, 96 +/- 7, and 68 degrees, respectively. In none of these pelvic features was AL 288-1 "intermediate" between pongids and H. sapiens. The anatomical peculiarities of the pelvis in AL 288-1 are explained primarily as the result of early adaptation to erect posture, which resulted in the reduction of the distance between the sacroiliac joint and the hip joint. As a consequence, the sacral promontory moved toward the pubic symphysis, and this resulted in shortening of the AP diameter and widening of the TR diameter at the pelvic inlet.     

Locomotor adaptations within the Cercopithecus Genus: a multivariate approach.

Multivariate analysis as a technique for investigating locomotor differentiation among primates has proven its power and usefulness in many studies on various skeletal dimensions. In these analyses primate genera were distributed and sometimes clustered in a manner that was interpretable based on current knowledge of gross locomotor differences. In an effort to advance our understanding of arboreality and terrestriality in primates, the present research involves a careful look for the most subtle morphological differences in locomotor behavior. It is believed that by looking at such subtle shape differences an understanding of what it means morphologically for a primate to be either more or less arboreal may be achieved. The species within the primate genus Cercopithecus were analyzed. This genus includes species which may be placed along a habitat (ground-living to tree-dwelling) or activity spectrum. The different habitats or activity patterns clearly require slight variations in patterns of movement, which in turn may require subtle structural adaptations. Multivariate analyses of 67 postcranial variables on seven species within the genus allowed detection of slight degrees of morphological variation. However, when morphological differences are small, size variance among specimens may take on an inflated importance. A substantial amount of work was devoted to finding the least biased method of removing size variance from the variables while incorporating a discrete size variable into the study. Using these transformed skeletal variables, interspecific groupings were discovered. Much of this infrastructure is then related to differing locomotor behavior and provides an insight into the fine structure of primate locomotor adaptation in an arboreal habitat.     

Comparative assessment of the ischial morphology of Victoriapithecus macinnesi

An almost complete primate ischium was recovered from middle Miocene (ca. 15 ma) deposits of Maboko Island (Kenya) in 1987. The specimen shows numerous similarities to the ischial morphology of extant cercopithecids and is attributed to Victoriapithecus macinnesi (Von Koenigswald, 1969), the early Old World monkey best known from Maboko Island. The Victoriapithecus ischium provides the first evidence of early Old World monkey pelvic girdle anatomy. The ischium is characterized by an obliquely oriented and broadly flaring tuberosity, a relatively small acetabulum with little ventrally directed curvature of its caudal portion, a long ischial body and a flange-like ischial spine positioned caudal to the rim of the acetabulum. In these features, Victoriapithecus most closely resembles the vervet monkey, Cercopithecus aethiops. The fossil specimen indicates that Victoriapithecus possessed ischial callosities, a mobile tail and adaptations for (possibly cursorial) quadrupedalism with an adducted posture of the thigh. The occurrence of ischial callosities in Victoriapithecus extends the documented antiquity of this feature in catarrhines by more than 12 million years and shows that the distinctive “sitting-sleeping” adaptations of Old World monkeys (Washburn, 1957) originated prior to the divergence of Colobinae and Cercopithecinae. Differences of developmental sequence and tissue composition indicate that the ischial pads of cercopithecids, hylobatids, and pongids may have arisen independently, through parallel evolution. Contrary to Strasser and Delson (1987), discontinuity of ischial callosities was probably the primitive condition for male cercopithecids.     

Fetal ultrasonography: biometric data from four African primate species

BACKGROUND: Nonhuman primates are raised in large numbers in research centers and zoos. Reproductive monitoring is required to improve breeding performances. Ultrasonography is a safe method to determine gestational age and to estimate the date of parturition. However only few data are available in nonhuman primates. METHODS: Fetal biometric data were obtained throughout pregnancy on four African primate species, namely chimpanzee, gorilla, mandrill and patas monkey. Measurements included biparietal diameter, transverse abdominal diameter, femur and humerus length, external interorbital diameter, and fetal heart rate. Curves established from these data were compared with previously published data in chimpanzees and gorillas and with those for humans and other closely related primate species. RESULTS: The curves for the different hominids were very similar, while those for mandrills more closely resembled baboons and data for patas monkeys were comparable to those for macaques. CONCLUSIONS: These data, by providing a tool to evaluate precise gestational age, will be useful for centers raising these four primate species.     

Evolution of the ischial spine and of the pelvic floor in the Hominoidea

Study of the pelvis in 143 different mammals reveals that in quadrupeds the ischial spines are barely noticeable and are located posteriorly near the sacrum. In humans, the ischial spines are prominent and more anteriorly located. As a consequence of their position and size, the ischial spines in humans become an obstacle to parturition. Herein a theory is proposed to account for what appears to be an incongruous development and orientation of the ischial spines in humans. The pelvic diaphragm is a vertical pelvic "wall" in tailed mammals and is composed of muscles involved mostly with the motion of the tail. In humans, the muscles of the pelvic diaphragm have a very different anatomical orientation. They form a horizontal pelvic "floor," and their functions are first to support the abdominopelvic organs and resist intra-abdominal pressure that is exerted from above, and second, as levator ani, to control the anal sphincter. In humans the muscles and fascias of the pelvic diaphragm are inserted on the ischial spines either directly or indirectly through the sacrospinous ligament and the tendinous arch of the pelvic fascia. The result is a medial pull on the ischial spines to produce a more rigid and narrower pelvic floor. An inconstant ossification center for the ischial spines make them more prominent. The backward tilt of the sacrum placed the bispinal line in a diameter position. Pongids and even fossil hominids occupy an intermediate position between tailed mammals and Homo sapiens. The present form of the pelvis in Homo sapiens may be determined by a significant genetic component but may also be partly acquired during childhood and adolescence.     

Morphometry and allometry of the primate humerus

The primate distal humerus has been used both in phylogenetic reconstruction and in assessing locomotor and postural adaptations. This study uses an allometric approach to predict locomotor patterns of extant primates regardless of phylogenetic position. By showing the relationship between form and function in living primate taxa it will be possible to use this data set to predict locomotor behavior of extinct primates. Several linear measurements were taken from the distal humerus of 71 extant primate species (anthropoids and prosimians). Allometric regressions of each measurement were performed with mandibular M₂ area as a surrogate for body size. These measurements were used to determine if significant differences in distal humerus morphology exist among locomotor groups. The results were then used to test several hypotheses about the relationship between humeral form and function. For example, the hypothesis that suspensory primates have a large medial epicondyle is confirmed; the hypothesis that terrestrial quadrupeds have a deep olecranon fossa could not be confirmed with quantitative data. In addition to this hypothesis testing, the residuals from the allometric regressions of the humeral measurements were used in a discriminant functions analysis to estimate locomotor behavior from distal humerus morphology. The discriminant functions analysis correctly reclassified 64/71 (90%) species.