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Rapid nonsynonymous evolution of the iron-sulfur protein in anthropoid primates.

Cytochrome c (CYC) and 9 of the 13 subunits of cytochrome c oxidase (complex IV; COX) were previously shown to have accelerated rates of nonsynonymous substitution in anthropoid primates. Cytochrome b, the mtDNA encoded subunit of ubiquinol-cytochrome c reductase (complex III), also showed an accelerated nonsynonymous substitution rate in anthropoid primates but rate information about the nuclear encoded subunits of complex III has been lacking. We now report that phylogenetic and relative rates analysis of a nuclear encoded catalytically active subunit of complex III, the iron-sulfur protein (ISP), shows an accelerated rate of amino acid replacement similar to cytochrome b. Because both ISP and subunit 9, whose function is not directly related to electron transport, are produced by cleavage into two subunits of the initial translation product of a single gene, it is probable that these two subunits of complex III have essentially identical underlying rates of mutation. Nevertheless, we find that the catalytically active ISP has an accelerated rate of amino acid replacement in anthropoid primates whereas the catalytically inactive subunit 9 does not.

Amino Acid Sequence↗

Canine sexual dimorphism in Egyptian Eocene anthropoid primates: Catopithecus and Proteopithecus.

Two very small late Eocene anthropoid primates, Catopithecus browni and Proteopithecus sylviae, from Fayum, Egypt show evidence of substantial sexual dimorphism in canine teeth. The degree of dimorphism suggests that these early anthropoids lived in social groups with a polygynous mating system and intense male-male competition. Catopithecus and Proteopithecus are smaller in estimated body size than any living primates showing canine dimorphism. The origin of canine dimorphism and polygyny in anthropoids was not associated with the evolution of large body size.

Animals↗

Anthropoid humeri from the late Eocene of Egypt.

A number of recent studies have, by necessity, placed a great deal of emphasis on the dental evidence for Paleogene anthropoid interrelationships, but cladistic analyses of these data have led to the erection of phylogenetic hypotheses that appear to be at odds with biogeographic and stratigraphic considerations. Additional morphological data from the cranium and postcranium of certain poorly understood Paleogene primates are clearly needed to help test whether such hypotheses are tenable. Here we describe humeri attributable to Proteopithecus sylviae and Catopithecus browni, two anthropoids from late Eocene sediments of the Fayum Depression in Egypt. Qualitative and morphometric analyses of these elements indicate that humeri of the oligopithecine Catopithecus are more similar to early Oligocene propliopithecines than they are to any other Paleogene anthropoid taxon, and that Proteopithecus exhibits humeral similarities to parapithecids that may be symplesiomorphies of extant (or "crown") Anthropoidea. The humeral morphology of Catopithecus is consistent with certain narrowly distributed dental apomorphies-such as the loss of the upper and lower second premolar and the development of a honing blade for the upper canine on the lower third premolar-which suggest that oligopithecines constitute the sister group of a clade containing propliopithecines and Miocene-Recent catarrhines and are not most closely related to Proteopithecus as has recently been proposed.

Animals↗

Basal anthropoids from Egypt and the antiquity of Africa's higher primate radiation.

Early anthropoid evolution in Afro-Arabia is poorly documented, with only a few isolated teeth known from before approximately 35 million years ago. Here we describe craniodental remains of the primitive anthropoid Biretia from approximately 37-million-year-old rocks in Egypt. Biretia is unique among early anthropoids in exhibiting evidence for nocturnality, but derived dental features shared with younger parapithecids draw this genus, and possibly >45-million-year-old Algeripithecus, into a morphologically and behaviorally diverse parapithecoid clade of great antiquity.

Animals↗

Paleontology. Shaking the earliest branches of anthropoid primate evolution.

Primates living today are believed to share a common ancestor that originated in either Africa or Asia. Fossil examples of such anthropoid ancestors have been found in both continents, so pushing back the origins to a single location has been controversial. In their Perspective, Jaeger and Marivaux discuss results reported in the same issue by Seiffert et al. that may put part of the controversy to rest. Seiffert et al. describe the earliest and most complete African anthropoid fossils from the Fayum desert region of Egypt. Cranial and dental fossils of two different small species were found, and their character, especially the features of the fossil teeth, suggests an ancient evolutionary history in Africa. At the same time, the phylogenetic analysis of Seiffert et al. is consistent with the view that African anthropoids immigrated from Asia at a very early date, probably before the late Paleocene (60 million years ago), possibly followed by later waves of immigration.

Africa↗

A new primate from the Middle Eocene of Myanmar and the Asian early origin of anthropoids.

A new genus and species of anthropoid primate, Bahinia pondaungensis gen. et sp. nov., is described from the Yashe Kyitchaung locality in the Late Middle Eocene Pondaung Formation (Myanmar). It is related to Eosimias, but it is represented by more complete remains, including upper dentition with associated lower jaw fragment. It is interpreted as a new representative of the family Eosimiidae, which corresponds to the sister group of the Amphipithecidae and of all other anthropoids. Eosimiidae are now recorded from three distinct Middle Eocene localities in Asia, giving support to the hypothesis of an Asian origin of anthropoids.

Animals↗

A trinucleotide repeat-associated increase in the level of Alu RNA-binding protein occurred during the same period as the major Alu amplification that accompanied anthropoid evolution.

Nearly 1 million Alu elements in human DNA were inserted by an RNA-mediated retroposition-amplification process that clearly decelerated about 30 million years ago. Since then, Alu sequences have proliferated at a lower rate, including within the human genome, in which Alu mobility continues to generate genetic variability. Initially derived from 7SL RNA of the signal recognition particle (SRP), Alu became a dominant retroposon while retaining secondary structures found in 7SL RNA. We previously identified a human Alu RNA-binding protein as a homolog of the 14-kDa Alu-specific protein of SRP and have shown that its expression is associated with accumulation of 3'-processed Alu RNA. Here, we show that in early anthropoids, the gene encoding SRP14 Alu RNA-binding protein was duplicated and that SRP14-homologous sequences currently reside on different human chromosomes. In anthropoids, the active SRP14 gene acquired a GCA trinucleotide repeat in its 3'-coding region that produces SRP14 polypeptides with extended C-terminal tails. A C-->G substitution in this region converted the mouse sequence CCA GCA to GCA GCA in prosimians, which presumably predisposed this locus to GCA expansion in anthropoids and provides a model for other triplet expansions. Moreover, the presence of the trinucleotide repeat in SRP14 DNA and the corresponding C-terminal tail in SRP14 are associated with a significant increase in SRP14 polypeptide and Alu RNA-binding activity. These genetic events occurred during the period in which an acceleration in Alu retroposition was followed by a sharp deceleration, suggesting that Alu repeats coevolved with C-terminal variants of SRP14 in higher primates.

Animals↗

Earliest record of a parapithecid anthropoid from the Jebel Qatrani formation, Northern Egypt.

A fifth anthropoid (= anthropoidean, simian or simiiform) genus and species from the late Eocene Fayum Quarry L-41, Abuqatrania basiodontos gen. et sp. nov., further augments the already remarkable primate diversity from this locality and provides the first convincing extension of the enigmatic family Parapithecidae into the oldest productive vertebrate fossil-bearing stratum of the Jebel Qatrani Formation. A. basiodontos exhibits no clear autapomorphies nor any apomorphies that are shared exclusively with any other parapithecid species, and it is most parsimoniously interpreted as the sister taxon of a Qatrania-Parapithecus-Apidium clade. Reevaluation of two contemporaries of A. basiodontos, Serapia and Arsinoea, suggests that neither genus should be ranked as a basal parapithecid. Serapia is more derived than primitive parapithecids in the morphology of the lower fourth premolar and exhibits greater overall similarity to Proteopithecus in cusp placement and the shape and proportions of its lower teeth; accordingly, we place Serapia in the family Proteopithecidae. Arsinoea is much more problematic and does not fit well with any hitherto known Afro-Arabian anthropoid group; we place this genus in a new anthropoid family, Arsinoeidae.

Animals↗

Tactile discrimination capacity in relation to size and organization of somatic sensory cortex in primates: I. Old-World prosimian, Galago; II. New-World anthropoids, Saimiri and Cebus.

Living primates vary considerably in brain organization, in sensorimotor and cognitive abilities, and in natural behavioral repertoires. Comparative studies of primary (SI) and secondary (SII) somatic sensory cortex of primates reveal major differences in the size and in the complexity of topographic projection patterns. The separate projections of the glabrous hand to SI cytoarchitectonic areas 3b and 1 described in the Old World (OW) anthropoid Macaca and in New World (NW) anthropoids Cebus, Saimiri, and Aotus are lacking in NW Saguinus and in the prosimian Galago. The relationship between the size and complexity of SI organization and tactile abilities is explored in this study of four species of primates--Galago, Macaca, Cebus, and Saimiri. These species were trained to discriminate between pairs of objects differing either in cross-sectional diameter (size) or surface roughness (texture). The course of acquisition of such tactile discrimination in normal Macaca and the nature of deficits following SI or SII removals are known. Selective lesions of either cytoarchitectonic area 1 or 2 in Macaca affect only texture or size discriminations, respectively. Removal of area 3b in SI, or of SII, in Macaca affects both size and texture capacities. The single projection of the glabrous hand to area 3b-1 of Galago led to our expectation that the capacity of Galago to discriminate textures would be more similar to an area 1-lesioned than to a normal Macaca. The substantial and persistent differences between Macaca and Galago on texture, but not size, tasks lend support to the view that the evolution of a second projection of the glabrous hand to area 1 in Macaca contributes to increased texture discrimination capacity. The similarity in multiple projection patterns of the glabrous hand to areas 3b and 1 in Macaca, Saimiri, and Cebus led us to expect greater correspondence in texture discrimination capacity between these three anthropoids than to Galago. Contrary to expectations, Saimiri and Cebus showed a tactile capacity more similar to Galago than to Macaca. Furthermore, the texture discrimination capacity of Cebus actually improved substantially after removal of area 1. This provides further evidence, together with the single SI hand area in NW Saguinus and Galago, that the separate cutaneous projections to area 1 in OW and NW primates are not homologous but evolved independently and possibly serve different tactile functions.

Animals↗

Preliminary examination of non-occlusal dental microwear in anthropoids: implications for the study of fossil primates.

Most studies of microscopic wear on non-human primate teeth have focused on the occlusal surfaces of molars. Recent analyses of the buccal surfaces of human cheek teeth have demonstrated an association between diet and dental microwear on the these surfaces as well. In the current study, we examine microwear on both the buccal and lingual surfaces of non-human primate molars to assess the potential of these surfaces to reveal information concerning anthropoid feeding behaviors. We compare frequency of microwear occurrence in 12 extant and 11 fossil anthropoid species. Among the living primates, the occurrence of microwear on nonocclusal surfaces appears to relate to both diet and degree of terrestriality. The implications of this research for the inference of feeding behaviors and substrate use in fossil cercopithecoids are discussed.

Analysis of Variance↗

Functional significance of cortical bone distribution in anthropoid mandibles: an in vitro assessment of bone strain under combined loads.

Local variation in cortical bone thickness in the postcanine mandibular corpus appears to be stereotypical among anthropoids. Specifically, at sections under the molars, lingually situated cortical bone is typically thinner than that along the lateral aspect. This pattern applies despite phylogenetic, dietary, and allometric differences among the anthropoids sampled to date. Demes et al. (Food Acquisition and Processing in Primates [1984] New York: Plenum Press, p. 369-390) employed a theoretical analysis of mastication in Gorilla and Homo to argue that this pattern could be explained with reference to biomechanical stresses. Specifically, they proposed that the combined effects of torsion and direct shear on the working-side corpus create a condition in which net stresses and strains are reduced along the lingual cortical plate. Demonstration of this effect would suggest a functional linkage between localized differences in bone mass and strain gradients in the facial skeleton. We conducted an empirical evaluation of the effects of the combined loads of torsion and direct shear in vitro on a sample of formalin-fixed human mandibles. Rosette strain gages were affixed to the lateral and medial aspects of the corpus in each specimen, and surface strains were recorded separately under controlled torsional and occlusal loads, and under simultaneous application of these loads. The hypothesis that lingual strains are reduced under combined twisting and occlusal loads was generally supported; however, we observed reduction in surface strains at some sites along the lateral aspect of the corpus under these combined loads as well. These unexpected findings are attributable to unanticipated loading conditions imposed by occlusal forces, which result from sources of stress in addition to direct shear. These experiments provide provisional support for the hypothesis that superposed sources of bone strain produce large strain gradients between buccal and lingual aspects of the mandibular corpus, and that local variation in bone mass may be associated with these gradients.

Animals↗

Polymorphic aspects of male anthropoid canines.

Interspecific variation in the architecture of male anthropoid maxillary canines is documented. Extant taxa are polymorphic, and most can be sorted into two major groupings based on quantitative measures of shape, distal edge sharpness, and interspecific changes in their linear dimensions (projection, mesiodistal length, and buccolingual breadth) relative to each other and to body mass (scaling). One group includes the great apes and ceboids; the other includes cercopithecoids and hylobatids. Statistically significant differences between these groups were found for canine shape, for trajectories of regressions for canine projection on canine length and canine breadth, and for canine projection and canine breadth relative to body mass. The data indicate that explantations of canine variation in male anthropoids must include a mechanical interpretation of form in addition to assessments of habitus, heritage, and body mass.

Animals↗

Polymorphic aspects of male anthropoid honing premolars.

A recent study has indicated that heritage may be an important component in explanations of interspecies variation in male anthropoid maxillary canines. To further test this hypothesis, comparative data for the maxillary canine's occlusal partner, the honing mandibular premolar, are presented. Relative to body mass, measurements of the honing premolar--length of the honing facet, mesiodistal length, and buccolingual breadth and shape (as expressed by the ratio of length to breadth)--show a similar but stronger heritage component than measurements of the maxillary canine. Results indicate that canine variation among male anthropoids has not yet been explained and that quantitative analyses of this issue will necessarily require a methodological approach which incorporates heritage as a factor.

Animals↗

Intrasexual competition and canine dimorphism in anthropoid primates.

A number of factors, including sexual selection, body weight, body-weight dimorphism, predation, diet, and phylogenetic inertia have been proposed as influences on the evolution of canine dimorphism in anthropoid primates. Although these factors are not mutually exclusive, opinions vary as to which is the most important. The role of sexual selection has been questioned because mating system, which should reflect its strength, poorly predicts variation in canine dimorphism, particularly among polygynous species. Kay et al. (1988) demonstrate that a more refined estimate of intermale competition explains a large proportion of the variation in canine dimorphism in platyrrhine primates. We expand their analysis, developing a more generalized measure of intermale competition based on the frequency and intensity of male-male agonism. We examine the relative influences of predation (inferred by substrate use), female body weight, body-weight dimorphism, diet, and sexual selection on the evolution of anthropoid canine dimorphism. Intermale competition is very strongly associated with canine dimorphism. Predation also has a marked effect on canine dimorphism, in that savanna-dwelling species consistently show greater canine dimorphism than other species, all other factors being held equal. Body-weight dimorphism is also strongly associated with canine dimorphism, though apparently through a common selective basis, rather than through allometric effects. Body weight seems to play only a minor, indirect role in the evolution of canine dimorphism. Diet plays no role. Likewise, we find little evidence that phylogenetic inertia is a constraint on the evolution of canine dimorphism.

Analysis of Variance↗

Canine size and shape in male anthropoid primates.

While studies of canine dimorphism in primates are common, only a few have examined canine tooth size independently within each sex. Recently, Greenfield and Washburn (Am. J. Phys. Anthropol. 84:17-34, 1991) proposed that there are two types of male canines which reflect different allometric scaling patterns of canine crown height against canine occlusal dimensions. They also suggest that proportional canine shape, measured as canine crown height (or projection) relative to the occlusal dimensions, provides an estimate of the canine's function as a weapon, though they provide no test of this hypothesis. This analysis critically examines the claim that there are two types of male canines among anthropoids. It then tests the hypothesis that relative male canine size (measured against body weight) and proportional canine shape are related to estimates of intermale competition, diet, and substrate (used as a surrogate measure of predation pressure). While there is strong taxonomic variation in canine size and shape among male anthropoids, no evidence is found for two discrete canine types. Rather, within families and subfamilies, canine dimensions scale isometrically against body weight and against each other, with a continuum of canine shapes among different taxa. While variation in male canine size is associated with intermale competition and substrate, even when taxonomic variation is controlled, variation in proportional canine shape is not. Neither canine size nor shape are generally associated with variation in diet.

Analysis of Variance↗

Incisor microwear of Sumatran anthropoid primates.

Several studies have suggested that incisor microwear reflects diet and feeding adaptations of anthropoids. However, such studies have been largely qualitative, and interpretations have relied on anecdotal references to diet and tooth use reported in the socioecology literature. The current study relates incisor microwear in four anthropoid primates to specific ingestive behaviors and food types. Central incisor casts of wild-shot museum specimens of Hylobates lar, Macaca fascicularis, Pongo pygmaeus, and Presbytis thomasi were examined by scanning electron microscopy, and analyzed using a semiautomated image analysis procedure. Microwear patterns were used to generate predictions regarding diet and anterior tooth use. These predictions were evaluated using data collected during a 1 year study of feeding behavior of these same taxa in the wild (Ungar, 1992, 1994a,b). Results suggest that (1) enamel prism relief is associated with the effectiveness of etching reagents in foods, (2) dental calculus buildup results from a lack of incisor use and perhaps the ingestion of sugar-rich foods, (3) striation density varies with degree of anterior tooth use in the ingestion of abrasive food items, (4) striation breadth is proposed to relate to the ratio of exogenous grit to phytoliths consumed; and (5) preferred striation orientation indicates the direction that food items are pulled across the incisors during ingestion. It is concluded that incisor microwear studies can contribute to the understanding of diets and feeding behaviors of extinct primates.

Analysis of Variance↗

Ontogenetic correlates of diet in anthropoid primates.

This study assesses ontogenetic correlates of diet in anthropoid primates. Associations between body weight growth, adult size, and diet are evaluated for a sample of 42 primate species, of which 8 are classifiable as "folivores." The hypothesis that folivores show a pattern of growth that differs from "nonfolivores" is tested. Ontogenetic variation is summarized through use of parametric and nonparametric regression analysis. Several analytical techniques, including broad interspecific and detailed comparisons among species of similar adult size, are applied. This investigation indicates a clear association between body weight ontogeny and diet: folivorous species grow more rapidly over a shorter duration than comprably sized nonfolivorus species. A positive correlation between adult size and diet is not unambiguously established in this sample. A threshold (at around 1 kg) below which insectivory is very common may adequately characterize the association between adult size and diet in anthropoid primates. Above this threshold, adult size does not appear to covary predictably with diet. Evolutionary correlates of the ontogenetic pattern seen in folivores may include a variety of factors. The distinctive pattern of development in folivores may relate to the profile of ecological and social risks that these species face. Morphophysiological advantages to rapid growth may relate to a need for accelerated alimentary (dental and gut) development. The implications of ontogenetic variation in folivores are discussed.

Age Factors↗

Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca.

As the first part of a comparative investigation of primate frontal cortex, we compared the frontal architectonic organization of Galago, a small-brained, strepsirhine (or "prosimian") primate, to that of an anthropoid primate, Macaca, by using myelin- and Nissl-stained material. We were able to distinguish many more areas in both taxa than have been recognized in most previous studies of the primate frontal lobe. In particular, we were able to subdivide many of the areas shown in the commonly cited architectonic map of Walker (J. Comp. Neurol. 73:59-86, 1940). Delineation of areas was greatly facilitated by the use of the Gallyas technique for staining myelin. The areal organization of much of frontal cortex (specifically, the premotor, orbital, and medial regions) appears to be very similar in Galago and Macaca. In these regions, we were able to recognize the same complement of areas in both taxa, with few exceptions. In the granular frontal cortex (GFC), by contrast, we were able to distinguish about twice as many areas in Macaca as in Galago. For most of the GFC areas of Galago, there are architectonically similar areas in Macaca; the areas shared by both taxa correspond mainly to the arcuate and superior areas of Macaca (i.e., the region encompassed by Walker's areas 45, 8A, and 8B). However, there are many additional, more rostral, areas in Macaca for which there are no obvious homologues in Galago. In particular, Galago lacks cortex resembling the distinctive, lightly myelinated cortex of the Macaca principal sulcus (Walker's area 46 and its subdivisions). Our results are difficult to reconcile with the view that frontal lobe organization varies little across taxa. Rather, they suggest that granular frontal cortex underwent considerable change during primate evolution, including the addition of new areas in anthropoids.

Animals↗