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The recognition and evaluation of homoplasy in primate and human evolution.

Homoplasy has been a prominent issue in primate systematics and phylogeny for as long as people have been studying human evolution. In the past, homoplasy, in the form of parallel evolution, was often considered the dominant theme in primate evolution. Today, it receives blame for difficulties in phylogenetic analysis, but is essential in the study of adaptation. This paper reviews the history of study of homoplasy, methods of defining homoplasy, and methodological and biological factors that generate homoplasy. A post hoc definition of homology and homoplasy, based on patterns of character distributions and their congruence or incongruence on a cladogram, is the most consistent method of recognizing these phenomena. Defined this way, homology and homoplasy are mutually exclusive. However, when different levels of analysis are examined, it is seen that homoplasy at one level, such as adult phenotype, often exists simultaneously with homology at a different level, such as developmental process. Thus, in some cases, patterns of homoplasy may point to underlying similarities that reflect the shared heritage of a particular clade. This is an old concept that is being renewed on the strength of recent trends in developmental biology. Factors that influence homoplasy include character definition and a host of biological factors, such as developmental constraints, allometry, and adaptation. These interact with one another to provide explanations of homoplastic patterns. Because of the repetition of events, explanations of homoplastic features are often more reliable than those for homologous features, and serve as effective tests for hypotheses of evolutionary process. In some cases, particular explanations of homoplasy lead to generalizations about the likelihood of homoplasy in a type of structure. The structure may be adaptive or highly epigenetic, or it may belong to an anatomical system considered to be more prone to homoplasy than others. However, our review shows that these generalizations are usually based on theory, and contradictory expectations can be developed under different theoretical models. More rigorous empirical studies are necessary to discover what, if any, generalizations can be made about the likelihood of homoplasy in different types of characters.

Adaptation, Physiological↗

Conservation and evolution of microsatellite loci in primate taxa.

Microsatellites are promising genetic markers for the study of demographic structure and phylogenetic history in populations. However, little information exists on the molecular nature of the repeats and their flanking sequences of a same microsatellite in a large range of species. In this study, we report polymorphism and consensus sequences of eight microsatellite loci using human primers in 20 primate species. The results show size polymorphism in almost all species and microsatellites. These loci are therefore useful markers for population genetic studies between populations of the same species. Insertion/deletion events are frequent in the flanking regions, the majority concerning several contiguous bases. This is in contrast with the more usual single base pair events in non-coding regions. The ranges of allele lengths in non-human primates often show no overlap with that of human, usually due to the deletion/insertion events in the flanking sequences, producing smaller allele lengths rather than smaller numbers of repeats. The use of length of PCR product will bias the inter-species interpretation reducing the number of observable alleles and treating as the same allele very divergent molecular sequences. Caution should be used when employing microsatellites in cross-species comparisons in which the species under study are separated by significant amounts of evolutionary time: in such cases allele comparison cannot be based on lengths alone.

Animals↗

The neurobiology of primate puberty.

In higher primates the protracted prepubertal phase of development is occasioned by a mechanism that suppresses pulsatile hypothalamic gonadotropin-releasing hormone (GnRH) secretion from late infancy until the onset of puberty and thereby guarantees, in the juvenile, the quiescence of the pituitary-gonadal axis. Studies from our laboratory have employed the rhesus monkey, a representative higher primate, as an experimental paradigm. GnRH release has been measured using luteinizing hormone secretion by the in situ pituitary as a bioassay for the hypothalamic hormone. The nature of the prepubertal brake on pulsatile GnRH release in the monkey has been probed using physiological, neuroanatomical and neuropharmacological approaches. Such studies have led to the view that the prepubertal hiatus in pulsatile GnRH release results from a withdrawal in late infancy of a synchronized frequency-facilitated afferent neural input to the GnRH network, which in all other respects appears to exhibit properties identical to those in the postpubertal animal. The mechanism timing the onset of puberty, i.e. that responsible for the reactivation of synchronous activity in the GnRH network, is posited to be under the control of a central neural time- or growth-tracking device.

Aging↗

Health evaluation of translocated free-ranging primates in French Guiana.

Among over 40 mammal species threatened by the filling of a hydroelectric dam reservoir in French Guiana, three species of primates have been translocated, comprising 124 red howler monkeys, six white-faced sakis, and 95 golden-handed tamarins. Health status of the animals was evaluated by direct physical examination and by hematological, biochemical, virological, and parasitological surveys of collected blood. The physical condition of the howlers was slightly worse toward the end of the capture period, but that of sakis and tamarins remained satisfactory. Several ectoparasites (ticks, larvae of dipterous insects, fleas, and lice) were collected, and various wounds, apparently nondebilitating, were recorded in howlers. Hematological and biochemical profiles determined for the three species revealed a slight anemia in howlers. Entamoeba, Strongyloides, and Trypanoxyurus were common in fecal samples of howlers. A survey of blood smears from the three species revealed infection by several types of microfilaria, Trypanosoma rangeli-like and Plasmodium brasilianum in all three, and Trypanosoma cruzi-like in howlers. These infections had no significant impact on the health status or the hematological profiles. Serologic investigations revealed occasional reactions against Toxoplasma gondii, a strong anti-Plasmodium response in the two Cebidae species, and a weaker one in tamarins. Attempts to isolate arbovirus failed, but antibody responses to Mayaro and yellow fever viruses were strong, especially in the howlers. A strong correlation between age and serological status led to a better understanding of the epidemic cycles. Our survey indicates French Guianan primates are reservoirs for several anthropozoonoses, including malaria, Chagas disease, and arboviruses.

Animal Diseases↗

Primate molar crown formation times and life history evolution revisited.

Comparative studies have convincingly demonstrated that the pattern and timing of tooth emergence are highly correlated with life-history variables and brain size. Conversely, a firm relationship between molar formation time and life-history variables has not yet been established. It seems counterintuitive that one aspect of dental development should be correlated with life-history variables, whereas the other should not. In order to shed light on this apparent discrepancy this study analyzed all data on primate molar crown formations available in the published literature in relation to life-history variables, brain size, and female body mass. Crown formation times were found to be particularly highly correlated with both female body mass and brain size. Species that depart from the overall brain/body allometry by being relatively large-bodied, e.g., Gorilla gorilla and later Theropithecus oswaldi, also have shorter molar crown formation times than expected. The reverse is not found for species that depart from the overall brain/body allometry due to their larger brains, i.e., Homo sapiens. This finding is interpreted within an evolutionary and ecological framework. Specifically, by focusing on ecological commonalities, a scenario is proposed which may allow predictions to be made about the evolutionary history of other extinct primates also. If confirmed in future studies, crown formation time may again become a powerful tool in evolutionary enquiry.

Animals↗

Sex identification assay useful in great apes is not diagnostic in a range of other primate species.

The ability to identify the sex of individuals from noninvasive samples can be a powerful tool for field studies. Amelogenin, a nuclear gene proximate to the pseudoautosomal region of mammalian sex chromosomes, has a 6 base-pair (bp) size difference between human X and Y chromosomes that can be PCR-amplified and sized to distinguish male from female DNA. We examined whether this test can be used to identify sex from different DNA sources across a number of nonhuman primate taxa. Using human amelogenin primers, we were able to amplify diagnostic products from the four great ape species tested, but products from five other primate species were not sexually dimorphic.

Amelogenin↗

Nonhuman primates and the acquired immunodeficiency syndrome: a union of necessity.

Because of the close phylogenetic relationship, nonhuman primates are highly susceptible to human pathogens, including infection of chimpanzees by the human immunodeficiency virus (HIV), the causative agent of AIDS. This, and the existence of a highly related simian virus, SIV, which causes an AIDS-like disease in macaques, emphasizes the continued importance of using nonhuman primates as model systems for identifying and developing prophylaxis and therapy for infectious agents and, in particular, for fighting the pandemic AIDS.

Acquired Immunodeficiency Syndrome↗

New perspectives in primate cognitive ecology.

The papers in this issue are from a symposium presented at the 71st Annual Meeting of the American Association of Physical Anthropologists held in Buffalo, New York, in April 2002. In the light of recent theoretical and methodological advances and debates in the study of cognition, this symposium addressed questions concerning primate cognitive ecology and decision-making from a variety of perspectives. These include ontogenetic patterns of brain growth and learning, paleoecology and evolution, sensory adaptations, foraging strategies, tool-using behavior, and concepts derived from the study of human cognition, such as schemata, planning, and rehearsal of activities. In this issue, data are presented on New World monkeys, Old World monkeys, apes, and humans. It is argued that the ability to make decisions based on the recognition that tertiary relationships in one context can be used to understand cause-and-effect relationships in an unrelated context may enable nonhuman primates to effectively reduce uncertainty and solve problems in changing social and ecological environments.

Animals↗

Accessory chemosignaling mechanisms in primates.

Accessory olfaction is defined as the chemoreceptive system that employs the vomeronasal complex (VNC) and its distinct central projections to the accessory olfactory bulb (AOB) and limbic/cortical systems. Comparisons of the structural and functional features of primate accessory olfaction can now be made at many levels. Advances in the understanding of molecular mechanisms of odorant transfer and detection, physiological analyses of signal processing, and appreciation of ontogenetic timetables have clarified the contribution of accessory chemoreception to the sensory map. Two principal functions dominate: the decoding of social information through the uptake of signals (often fluid-borne), and the provision of an essential pathway for the "migration" of presumptive neurocrine (GnRH) cells from the olfactory placode to the hypothalamus. VN "smelling" (vomerolfaction) is now seen to overlap with primary olfaction. Both systems detect signal compounds along the spectrum of volatility/molecular weight, and neither is an exclusive sensor. Both main and accessory chemoreception seem to require collaborative molecular devices to assist in odorant transfer (binding proteins) and (for the VNO) signal recognition (MHC1 proteins). Most adaptive-selective features of primate chemocommunication variously resemble those of other terrestrial mammals. VN function, along with its genome, has been maintained within the Strepsirrhines and tarsiers, reduced in Platyrrhines, and nearly extinguished at the Catarrhine up to hominin levels. It persists as an intriguing ancient sense that retains key features of past evolutionary events.

Animals↗

Olfactory evolution and behavioral ecology in primates.

Primates are usually thought of as "visual" mammals, and several comparative studies have emphasized the role of vision in primate neural and sociocognitive specialization. Here I explore the role of olfactory systems, using phylogenetic analysis of comparative volumetric data. The relative sizes of the main olfactory bulb (MOB) and accessory olfactory bulb (AOB) tend to show different evolutionary patterns in accordance with their different functions. Although there is some evidence of correlated evolution of the two systems, this is apparent in only one clade (the strepsirhines). As predicted, the MOBs correlate predominantly with ecological factors (activity period and diet), while the AOBs correlate with social and mating systems. Related olfactory structures (i.e., the piriform cortex and amygdala) exhibit correlated evolution with the AOBs but not with the MOBs, and the corticobasolateral part of the amygdala exhibits a correlation with social group size in platyrrhines similar to that observed for the AOB. These social system correlations support the idea that there is an olfactory dimension to the concept of the social brain.

Animal Communication↗

Three-dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography.

Until recently, detailed analyses of the architecture of nonhuman primate cancellous bone have not been possible due to a combination of methodological constraints, including poor resolution imaging or destructive protocols. The development of micro-computed tomography (microCT) and morphometric methods associated with this imaging modality offers anthropologists a new means to study the comparative architecture of cancellous bone. Specifically, microCT will allow anthropologists to investigate the relationship between locomotor behavior and trabecular structure. We conducted a preliminary study on the trabecular patterns in the proximal humerus and femur of Hylobates lar, Ateles paniscus, Macaca mulatta, and Papio anubis to investigate the quantitative differences in their trabecular architecture and evaluate the potential of microCT in anthropological inquiry. MicroCT allows the researcher to evaluate variables beyond simple two-dimensional orientations and radiographic densities. For example, this methodology facilitates the study of trabecular thickness and bone volume fraction using three-dimensional data. Results suggest that density-related parameters do not reliably differentiate suspensory-climbing species from quadrupedal species. However, preliminary results indicate that measurements of the degree of anisotropy, a measure of trabecular orientation uniformity, do distinguish suspensory-climbing taxa from more quadrupedal species. The microCT method is an advance over conventional radiography and medical CT because it can accurately resolve micron-sized struts that make up cancellous bone, and from these images a wide array of parameters that have been demonstrated to be related to cancellous bone mechanical properties can be measured. Methodological problems pertinent to any comparative microCT study of primate trabecular architecture are discussed.

Animals↗

Field methodology for lateral cranial radiography of nonhuman primates.

The historical lack of field-based radiographic studies of nonhuman primates within the field of anthropology is likely due to the perceived difficulty of transporting and operating X-ray equipment. Here we present a method for taking lateral cranial radiographs of nonhuman primates in the field that is simple to employ, and that produces exposed films suitable for collection of measurement data useful for growth and development studies, as well as for investigating bone and soft-tissue pathology. Several different X-ray units, film types, and portable power sources were used, all producing suitable images of similar quality, indicating that this methodology is likely not overly sensitive to these important parameters.

Animals↗

Phylogenetic implications of comparative primate growth rates.

Growth data from a number of species of Old and New World primates have been analyzed by calculating instantaneous relative growth rates. Species discussed are the New World species Saimiri sciureus and Saguinus nigricollis, and the Old World species Pan troglodytes and Macaca mulatta. The analysis of the perinatal growth data indicated that differences in relative growth rates are present during early periods of growth. More specifically, it was found that the closer taxonomically a species is to man the greater the deceleration of growth during the first postnatal year. It is suggested that this may be a general primate trend.

Age Factors↗

Mineral metabolism and microstructural defects in primate teeth.

There are numerous structural defects that occur in primate teeth due to variable calcification during certain growth stages. These interruptions are usually areas of hypomineralization in enamel and dentin which are referred to as Striae of Retzius and Hunter Shreger bands in the enamel or Incremental Lines of von Ebner and Contour Lines of Owen in the case of the dentin. The frequency of occurrence of these variations in mineralization can be related to such factors as growth tempo, dietary quality, state of health, and past disease episodes. Another structure that appears in the dentin is a region that fails to calcify and is referred to as Inter-globular Dentin. Our studies have shown that the microstructural quality of different species' dentition varies widely. Samples obtained from certain fre-ranging cercopithcoids show that these species have the least hypomineralizations while man has the most. Other primate species range between these two extremems with the pongids nearer to man in these characteristics, as previously noted by Sognnaes. Additionally, out initial study shows a great deal of diversity between prehistoric human populations in the microstructural quality of their teeth. We offer the tentative explanation that this variation is due to differences in the calcitying properties of the diet and hence a difference in the general state of their health.

Adolescent↗

Functional implications of primate enamel thickness.

Recent evolutionary interpretations of Hominoidea have postulated functional relationships between tooth form, diet and masticatory biomechanics. A major consideration is the durability of the tooth under certain dietary conditions. Teeth with low cusps and thicker enamel are able to withstand heavy mastication of abrasive food bolus for a longer period. When comparisons are made between species of higher primates the variables of tooth size, cusp morphology, and enamel thickness appear to be related but until now no systematic analysis has been made to determine the functional relevance of several dental dimensions. This study provides data gained from comparisons of dentition of nine species of primates. Histological sections were made of the post canine teeth and 21 dimensions were compared. The relevant dimensions identified serve to withstand dental wear. The distribution of thicker enamel corresponded to the observed wear planes. Humans had thicker enamel than pongids while the macaque had the thinnest. These preliminary results tend to support theories which explain low, thick, enameled cusps in hominids.

Animals↗

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.

Animals↗

Supernumerary molars in Anthropoidea, Adapidae, and Archaeolemur: implications for primate dental homologies.

The model of primate dental homologies and development recently proposed by Schwartz ('75, '78) is re-evaluated in view of documented exceptions to his account of postcanine supernumerary teeth in both anthropoids and prosimians. Schwartz concluded that catarrhines and living indriids retain only two true molars in each dental quadrant. As many as six molars on one side of the jaw can develop in rare instances in catarrhines, and supernumerary molars are also known for a wide range of other primates, including Cebidae, Adapidae, and subfossil Indriidae. Polydontia cannot be explained exclusively by atavistic development. More convincing explanations regard supernumerary teeth as the result of excessive growth of the dental lamina or localized twinning of tooth buds during early development. Conventional dental formulae of catarrhines and indriids including three permanent molars remain the most plausible.

Animals↗

Quantitative differences in dental microwear between primate species with different diets and a comment on the presumed diet of Sivapithecus.

Studies of dental microwear have been used to relate tooth form to function in a variety of recent and extinct mammals. Probably the most important aspect of microwear analysis is the possibility of using it to deduce the diet of extinct animals. Such deductions must be based on comparative studies of modern species with known diets, but to date, only qualitative studies have been attempted and all have been based on small samples. Here we report quantitative differences in dental microwear between primate species that are known to have different diets. Occlusal facets with different functions have previously been shown to exhibit different microwear patterns. However, the differences between facets of one species are shown to be far less than those between homologous facets of different species. Study of seven species of extant primates shows that enamel microwear can be used to distinguish between those with a mainly frugivorous diet and those with a mainly folivorous one. Microwear can also distinguish hard-object feeders from soft-fruit eaters. The microwear of Miocene Sivapithecus indicus cannot be distinguished statistically from that of the chimpanzee, but it is different from that of the other species. On this evidence S. indicus was not a hard-object feeder and the adaptive significance of its thick molar enamel is at present unknown.

Animals↗