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Functional osteology of the primate carpus with special reference to strepsirhini.

Preuschoft et al. ([1993] in H. Preuschoft and D. Chivers (eds): Hands of Primates. New York: Springer-Verlag, pp. 245-256) used a theoretical biomechanical analysis to generate several predictions relating subordinal differences in primate hand proportions to differences in carpal morphology. This study tests these predictions using quantitative analyses of carpal morphology between extant haplorhine and strepsirhine primates. Results show that living strepsirhines have a significantly larger hamate hamulus than do haplorhines, supporting a Preuschoft et al.'s (1993) predictions. Extant strepsirhines also have a significantly shorter pisiform body than do haplorhines and arboreal nonprimate eutherians and a larger scaphoid tubercle than new and Old World monkeys. These results contrast markedly with those expected under Preuschoft et al.'s (1993) model. Furthermore, strepsirhines and haplorhines do not differ significantly in the relative size of their radiocarpal articulations. These morphometric observations do not match the predicted morphological patterns because the kinematic assumptions upon which the biomechanical models are based are incorrect. Living strepsirhines appear to be derived in having very deep radial and ulnar margins of the carpal tunnel for well-developed extrinsic digital flexors. Moreover, tooth-combed prosimians differ from most haplorhines, early Tertiary adapiforms, and arboreal nonprimate eutherians in having a relatively short pisiform body, which gives the flexor carpi ulnaris less power to flex the wrist from extended (= dorsiflexed) positions. These structural observations suggest that powerful manual grasping and an emphasis on leaping and climbing, rather than palmigrade quadrupedal walking and running, are morphotypic for extant Strepsirhini.

Animals↗

The ovoimplantation of Microcebus murinus Miller. (Primates, Lemoruoidea, Strepsirhini).

The process of nidation of Microcebus murinus may be subdivided into several stages (preadhesion, apposition, attachment and invasion), as is indicated for protracted phases of preimplantation. Not until the apposition stage does the inner cell mass orient itself orthomesometrially, while concurrently a nidation plaque develops in the abembryonal trophoblast that overlies and resorbs the coalescent glands. During the subsequent adhesion stage, the paraembryonal, bilaminar omphalochorion becomes attached to the uterine epithelium, with focal resorption of the latter. In addition, chorionic vesicles begin to develop. In the meantime, the embryonic disc has lost its trophoblastic cover as a preliminary to the formation of the pleuramnion. The formation of a nidation plaque, together with the subsequent central implantation of Microcebus, suggests a close relationship to Loris tardigradus, characterizing the mode of implantation of Strepsirhini. The nidation plaque and its invasive capacity, giving rise to a syndesmochorial placental nucleus, provide a placentological link to Galago demidovii.

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Phylogenetic relationships among Indriidae (Primates, Strepsirhini) inferred from highly repeated DNA band patterns.

Comparative studies of highly repeated DNA from different species of Indriidae (Primates, Strepsirhini) allowed confirmation of the specific status of Avahi occidentalis, A. laniger and Propithecus tattersalli. The comparison of their band patterns revealed the existence of specific and common bands from which a cladogram of the family is inferred. This cladogram shows that Avahi clade is the sister-group of Indri and Propithecus clade, and that P. verreauxi is related to P. diadema. These results were discussed in view of those obtained from cytogenetic, morphological and molecular data (mitochondrial DNA). This study shows the capacity of the repeated sequence pattern comparison to be used as a tool for confirming taxa status, (taxinomic classification is a primary determinant of management priorities for endangered species, neglect of distinct taxa may lead to their extinction), and for inferring phylogenetic relationships among related species.

Animals↗

Immunodiffusion systematics of the primates. III. The strepsirhini.

Immunodiffusion comparisons have been run using 26 antisera including seven made to strepsirhine species. Spur size data resulting from these comparisons have been analyzed by computer and depict Strepsirhini as a monophyletic group within Primates including Lemuriformes and Lorisiformes. Cheirogaleidae is retained with Lemuriformes. Indriidae rather than Cheirogaleidae is depicted as closer to Lemur. Evidence is presented indicating that Lorisiformes is composed of three groups rather than two as in traditional classifications. The three groups, which are considered here to diverage at a family level, are Galagidae, Lorisidae, and Perodicticidae.

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Localization of a new highly repeated DNA sequence of Lemur cafta (Lemuridae, Strepsirhini).

We have isolated and cloned an 800-bp highly repeated DNA (HRDNA) sequence from Lemur catta (LCA) and described its localization on LCA chromosomes. Lemur catta HRDNA sequences were localized by performing FISH experiments on standard and elongated metaphasic chromosomes using an LCA HRDNA probe (LCASAT). A complex hybridization pattern was detected. A strong pericentromeric hybridization signal was observed on most LCA chromosomes. Chromosomes 7 and 13 were lit in pericentromeric regions, as well as in the interspersed heterochromatin. Chromosomes 1, 3, 4, 17, 19, X, and microchromosomes (20, 25, 26, and 27) showed no signals in the pericentromeric region, but chromosomes 3 and 4 showed a positive hybridization in heterochromatic regions. The 800-bp L catta HRDNA was species specific. We performed FISH experiments with the LCASAT probe on Eulemur macaco macaco (EMA) and Eulemur fulvus fulvus (EFU) metaphases and no positive signal of hybridization was detected. These findings were also confirmed by Southern blot analysis and PCR.

Animals↗

Molecular evidence on primate phylogeny from DNA sequences.

Evidence from DNA sequences on the phylogenetic systematics of primates is congruent with the evidence from morphology in grouping Cercopithecoidea (Old World monkeys) and Hominoidea (apes and humans) into Catarrhini, Catarrhini and Platyrrhini (ceboids or New World monkeys) into Anthropoidea, Lemuriformes and Lorisiformes into Strepsirhini, and Anthropoidea, Tarsioidea, and Strepsirhini into Primates. With regard to the problematic relationships of Tarsioidea, DNA sequences group it with Anthropoidea into Haplorhini. In addition, the DNA evidence favors retaining Cheirogaleidae within Lemuriformes in contrast to some morphological studies that favor placing Cheirogaleids in Lorisiformes. While parsimony analysis of the present DNA sequence data provides only modest support for Haplorhini as a monophyletic taxon, it provides very strong support for Hominoidea, Catarrhini, Anthropoidea, and Strepsirhini as monophyletic taxa. The parsimony DNA evidence also rejects the hypothesis that megabats are the sister group of either Primates or Dermoptera (flying lemur) or a Primate-Dermoptera clade and instead strongly supports the monophyly of Chiroptera, with megabats grouping with microbats at considerable distance from Primates. In contrast to the confused morphological picture of sister group relationships within Hominoidea, orthologous noncoding DNA sequences (spanning alignments involving as many as 20,000 base positions) now provide by the parsimony criterion highly significant evidence for the sister group relationships defined by a cladistic classification that groups the lineages to all extant hominoids into family Hominidae, divides this ape family into subfamilies Hylobatinae (gibbons) and Homininae, divides Homininae into tribes Pongini (orangutans) and Hominini, and divides Hominini into subtribes Gorillina (gorillas) and Hominina (humans and chimpanzees). A likelihood analysis of the largest body of these noncoding orthologues and counts of putative synapomorphies using the full range of sequence data from mitochondrial and nuclear genomes also find that humans and chimpanzees share the longest common ancestry.

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Birth of a gene: locus of neuronal BC200 snmRNA in three prosimians and human BC200 pseudogenes as archives of change in the Anthropoidea lineage.

The gene encoding brain-specific dendritic BC200 small non-messenger RNA is limited to the primate order and arose from a monomeric Alu element. It is present and neuronally expressed in all Anthropoidea examined. By comparing the human sequence of about 13.2 kb with each of the prosimian (lemur 14.6 kb, galago 12 kb, and tarsier 13.8 kb) orthologous loci, we could establish that the BC200 RNA gene is absent from the prosimian lineages. In Strepsirhini (lemurs and lorises), a dimeric AluJ-like element integrated very close to the BC200 insertion point, while the corresponding tarsier region is devoid of any repetitive element. Consequently, insertion of the Alu monomer that gave rise to the BC200 RNA gene must have occurred after the anthropoid lineage diverged from the prosimian lineage(s). Shared insertions of other repetitive elements favor proximity of simians and tarsiers in support of their grouping into Haplorhini and the omomyid hypothesis. On the other hand, the nucleotide sequences in the segment that is available for comparison in all four species reveal less exchanges between Strepsirhini (lemur and galago) and human than between tarsier and human. Our data imply that the early activity of dimeric Alu sequences must have been concurrent with the activity of monomeric Alu elements that persisted longer than is usually thought. As BC200 RNA gave rise to more than 200 pseudogenes, we used their consensus sequence variations as a molecular archive recording the BC200 RNA sequence changes in the anthropoid lineage leading to Homo sapiens and timed these alterations over the past 35-55 million years.

Alu Elements↗

Morphometrics of the anterior dentition in strepsirhine primates.

Size variations in the anterior dentition were analyzed for 26 species of strepsirhine primates. The upper and lower incisor rows of strepsirhines, like those of anthropoid primates, scale isometrically with body size. Within the order Primates, strepsirhines exhibit the smallest incisors relative to body size, followed in increasing size by tarsiers, platyrrhines, and catarrhines. If the lateral teeth of the indriid toothcomb are interpreted as incisors and not canines, correlations between mandibular tooth size variables and body weight are maximized. The upper incisors of strepsirhines are extremely small and frequently widely separated, most likely to minimize occlusion with the toothcomb. Species deviations for assorted size variables of the anterior dentition generally fail to reflect functional variations in the use of the anterior teeth; some of the variables, however, do reflect taxonomic differences within the Strepsirhini. Although toothcomb size variations among extant strepsirhines are more readily interpreted in terms of gum feeding and bark scraping than they are in terms of grooming, anterior dental morphology as a whole is more easily explained by a grooming hypothesis when existing models of toothcomb origins are considered.

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Retinal projection to the olfactory tubercle and basal telencephalon in primates.

The retinal projection to the basal telencephalon was studied in eight species of primates from the suborders Strepsirhini and Haplorhini, including one anthropoid primate, the gibbon. Animals received an intraocular injection of tritiated amino acids and the distribution of retinal fibers and terminals was demonstrated by autoradiographic techniques in horizontal and coronal sections. In all species a discrete group of labeled retinal fibers is observed to branch off from the dorsolateral aspect of the optic tract at the level of the suprachiasmatic nucleus. These fibers, destined to the basal telencephalon, are topographically distinct from the retinal fibers which innervate the suprachiasmatic nucleus and medial hypothalamic regions. The fibers of the retinotelencephalic tract course dorsally above the supraoptic nucleus through the lateral hypothalamic area and then proceed further rostrally and laterally below the diagonal band of Broca towards the olfactory tubercle. Within the olfactory tubercle, terminal distribution of label is observed in the mediocaudal region along the granular cell layer II. In the macaque this cellular layer shows a characteristic thickening in the region of retinal terminals which is evident in both coronal and horizontal section. In some species this labeled region is seen within the superficial bulge of the tubercle on the ventral aspect of basal telencephalon. In all primates the retinal projection to olfactory tubercle is bilateral. In prosimians label is predominantly contralateral to the injected eye, in New World monkeys label is equally distributed on both sides of the brain and in Old World monkeys label is mainly found ipsilaterally. Retinal fibers were also seen in the periamygdaloid region but never extended as far as piriform cortex. These results, in addition to previous studies in other mammalian orders, confirm that the basal telencephalon, and in particular the olfactory tubercle, constitutes a region of visual and olfactory convergence. This sensory integration may be related to photic and chemosensory modulation of reproductive physiology and behavior.

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Primate phylogeny: morphological vs. molecular results.

Our comparative study of morphological (our data on selected living primates) and molecular characters (from the literature) confirms that, overall, phylogenetic reconstructions of Primates, and consequently their classifications, are more similar than dissimilar. When data from fossil Primates are incorporated, there may be several possible relationships among living Primates; the difference between most of them hinges mainly on the position of Tarsius. In one hypothesis, tarsiers are closely related to lemurs and lorises, and thus Primates is divided into Prosimii [lorises, lemurs, and tarsiers] and Anthropoidea [Platyrrhini and Catarrhini, i.e., monkeys, apes, and humans]. Two additional alternatives are that Tarsius is a sister group to the clade embracing lorises + lemurs and Anthropoidea and that in which all three lineages (Tarsius, lorises + lemurs, and Anthropoidea) form a polychotomy. In another hypothesis, tarsiers are closely related to anthropoids, giving these two branches: Strepsirhini [lemurs, lorises] and Haplorhini [tarsiers and Anthropoidea (Platyrrhini, the New World monkeys, and Catarrhini, Old World monkeys and Hominoidea)]. The first three alternatives gain some support from the fossil record, and the fourth from morphology of the living Tarsius and molecular data. It is emphasized that the morphological characters employed in this study for Tarsius are based on the only surviving genus of once-diverse tarsiiform primates known from the Eocene, and, although considered a "living fossil," it cannot represent all of them. Furthermore, Tarsius embodies derived features of its own which may affect its systematic position, but not necessarily the position of Tarsiiformes. Although the early Tertiary adapoids might have more nearly resembled anthropoids in their biochemistry and placental developments, this hypothesis is not testable from fossils, and any inferred relationships here must be based on characters of skeletal anatomy. Alternatively, anthropoids may be derived from certain omomyids or from some as yet undiscovered Eocene African taxon. Close relationships among Homo, Pan, and Gorilla have been confirmed during recent decades; Pongo is the sister group to this trichotomy. With increasing molecular data, Homo and Pan appear to be closer to each other than to any other living hominid taxon. Gorilla is a sister group to the Homo-Pan clade and Pongo is a sister group to all of them. Morphologists have given limited evidence for such a dichotomous grouping. In this study, we support the Homo-Pan clade, although with characters not as strong as for other clades.

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Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence.

A highly resolved primate cladogram based on DNA evidence is congruent with extant and fossil osteological evidence. A provisional primate classification based on this cladogram and the time scale provided by fossils and the model of local molecular clocks has all named taxa represent clades and assigns the same taxonomic rank to those clades of roughly equivalent age. Order Primates divides into Strepsirhini and Haplorhini. Strepsirhines divide into Lemuriformes and Loriformes, whereas haplorhines divide into Tarsiiformes and Anthropoidea. Within Anthropoidea when equivalent ranks are used for divisions within Platyrrhini and Catarrhini, Homininae divides into Hylobatini (common and siamang gibbon) and Hominini, and the latter divides into Pongina for Pongo (orangutans) and Hominina for Gorilla and Homo. Homo itself divides into the subgenera H. (Homo) for humans and H. (Pan) for chimpanzees and bonobos. The differences between this provisional age related phylogenetic classification and current primate taxonomies are discussed.

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Evidence on primate phylogeny from epsilon-globin gene sequences and flanking regions.

Phylogenetic relationships among various primate groups were examined based on sequences of epsilon-globin genes. epsilon-globin genes were sequenced from five species of strepsirhine primates. These sequences were aligned and compared with other known primate epsilon-globin sequences, including data from two additional strepsirhine species, one species of tarsier, 19 species of New World monkeys (representing all extant genera), and five species of catarrhines. In addition, a 2-kb segment upstream of the epsilon-globin gene was sequenced in two of the five strepsirhines examined. This upstream sequence was aligned with five other species of primates for which data are available in this segment. Domestic rabbit and goat were used as outgroups. This analysis supports the monophyly of order Primates but does not support the traditional prosimian grouping of tarsiers, lorisoids, and lemuroids; rather it supports the sister grouping of tarsiers and anthropoids into Haplorhini and the sister grouping of lorisoids and lemuroids into Strepsirhini. The mouse lemur (Microcebus murinus) and dwarf lemur (Cheirogaleus medius) appear to be most closely related to each other, forming a clade with the lemuroids, and are probably not closely related to the lorisoids, as suggested by some morphological studies. Analysis of the epsilon-globin data supports the hypothesis that the aye-aye (Daubentonia madagascariensis) shares a sister-group relationship with other Malagasy strepsirhines (all being classified as lemuroids). Relationships among ceboids agree with findings from a previous epsilon-globin study in which fewer outgroup taxa were employed. Rates of molecular evolution were higher in lorisoids than in lemuroids.

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"Rodent-like" and "primate-like" types of astroglial architecture in the adult cerebral cortex of mammals: a comparative study.

Previous observations disclosed that astroglia with interlaminar processes were present in the cerebral cortex of adult New and Old World monkeys, but not in the rat, and scarcely in the prosimian Microcebus murinus. The present report is a more systematic and comprehensive comparative analysis of the occurrence of such processes in the cerebral cortex of several mammalian species. Brain samples were obtained from adult individuals from the following orders: Carnivora (canine), Rodentia (rat and mouse), Marsupialia (Macropus eugenii), Artiodactyl (bovine and ovine), Scandentia (Tupaia glis), Chiroptera (Cynopteris horsfieldii and C. brachyotis), and Primate: Prosimian (Eulemur fulvus), non-human primate species (Cebus apella, Saimiri boliviensis, Callithrix, Macaca mulatta, Papio hamadryas, Macaca fascicularis, Cercopithecus campbelli and C. ascanius) and from a human autopsy. Tissues were processed for immunocytochemistry using several antibodies directed against glial fibrillary acidic protein (GFAP), with or without additional procedures aimed at the retrieval of antigens and enhancement of their immunocytochemical expression. The cerebral cortex of non-primate species had an almost exclusive layout of stellate astrocytes, with only the occasional presence of long GFAP-IR processes in the dog that barely crossed the extent of lamina I, which in this species had comparatively increased thickness. Species of Insectivora and Chiroptera showed presence of astrocytes with long processes limited to the ventral basal cortex. Interlaminar GFAP-IR processes were absent in Eulemur fulvus, at variance with their limited presence and large within- and inter-individual variability as reported previously in Microcebus murinus. In New World monkeys such processes were absent in Callithrix samples, at variance with Cebus apella and Saimirí boliviensis. Overall, the expression of GFAP-IR interlaminar processes followed a progressive pattern: bulk of non-primate species (lack of interlaminar processes)--Chiroptera and Insectivora (processes restricted to allocortex) < strepsirhini < haplorhini (platirrhini < catarrhini). This trend is suggestive of the emergence of new evolutionary traits in the organization of the cerebral cortex, namely, the emergence of GFAP-IR long, interlaminar processes in the primate brain. Interlaminar processes may participate in a spatially restricted astroglial role, as compared to the one provided by the astroglial syncytium. It is proposed that the widely accepted concept of an exclusively astroglial syncytium is probably linked with a specific laboratory animal species ("rodent-type" or, rather, "general mammalian-type" model) that misrepresents the astroglial architecture present in the cerebral cortex of most anthropoid adult primates ("primate-type" model), including man.

Aged↗

Frequent segmental sequence exchanges and rapid gene duplication characterize the MHC class I genes in lemurs.

Major histocompatibility complex (MHC) class I genes have complicated and profound evolutionary histories. To reconstruct and better understand their histories, partial class I genes (exon 2-intron 2-exon 3) were sequenced in a sampling of prosimians (Strepsirhini, Primates). In total, we detected 117 different sequences from 36 Malagasy prosimians (lemurs) and 1 non-Malagasy prosimian (galago) representing 4 families, 7 genera, and 13 species. Unlike the MHC class II genes ( MHC-DRB), MHC class I genes show a generally genus-specific mode of evolution in lemurs. Additionally, no prosimian class I loci were found to be orthologous to HLA genes, even at highly conserved loci (such as HLA-E, HLA-F). Phylogenetic analysis indicates that nucleotide diversity among loci was very small and the persistence time of the polymorphisms was short, suggesting that the origin of the lemur MHC class I genes detected in this study was relatively recent. The evolutionary mode of these genes is similar to that of classic HLA genes, HLA-A, HLA-B, and HLA-C, in terms of their recent origin and rarity of pseudogenes, and differs from them with respect to the degree of gene duplications. From the viewpoint of MHC genes evolution, some interlocus sequence exchanges were apparently observed in the lemur lineage upon phylogenetic and amino acid motif analyses. This is also in contrast to the evolutionary mode of HLA genes, where intralocus exchanges have certainly occurred but few interlocus exchanges have taken place. Consequently, the gene conversion model for explaining the generation of the MHC diversity among different loci can be thought to play more important roles in the evolution of lemur MHC class I genes than in that of HLA genes.

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Sequence evolution, processing, and posttranslational modification of zonadhesin D domains in primates, as inferred from cDNA data.

Zonadhesin is a mammalian transmembrane sperm ligand. Precursor zonadhesin essentially consists of MAM (meprin/A5 antigen/mu receptor tyrosine phosphatase) domains, a mucin-like repeat, and D domains (homologous to von Willebrand D). Recent immunovisualization and binding assays indicate that zonadhesin D domains 1-3 bind postacrosomally to the zona pellucida. This feature has attracted considerable interest in the evolution of zonadhesin and its possible biological and biomedical implications. Previous molecular evolutionary analyses, however, were confined to cDNA sequences of only few distantly related species. Moreover, except for rabbit and pig, little is known about zonadhesin's processing. To delineate the situation in primates including humans, we analyze here the evolution of zonadhesin on the basis of D domain encoding cDNAs of about 4900 base pairs (bp) length from a representative primate sampling (1 Strepsirhini, 3 Cercopithecidae, 3 Platyrrhini, and human; 7 new sequences) plus GenBank data from mouse, rabbit, and pig. Site-specific (CODEML and HyPhy) analysis indicates positive evolution of zonadhesin. Moreover, moving window analysis (CRANN) points to a positive correlation of sequence evolution and sperm-competition. Significant accumulations of positively selected sites across interspecifically variable motifs (identified by PROSITE) suggest that positive selection promotes differences between species by amino acid exchanges and changes in posttranslational modification. In the case of zonadhesin D domains, positive selection might thus contribute to the species-specific binding of zonadhesin and zona pellucida. A high conservation of processing and dimerization motifs of primate zonadhesin in analogy to pig, on the other hand, illustrates that zonadhesin's backbone needs to meet basic requirements in order to retain function.

Amino Acid Sequence↗

Primates and their pinworm parasites: the cameron hypothesis revisited.

A morphologically based cladistic analysis of the Enterobiinae, which includes most of the Oxyuridae parasitic in Primates, allows a reevaluation of the Cameron's hypothesis of close coevolution with cospeciation between hosts and parasites. Each of the three genera separated in the Enterobiinae fits with one of the suborders defined in Primates: Lemuricola with the Strepsirhini, Trypanoxyuris with the Platyrrhini, and Enterobius with the Catarrhini. Inside each of the three main groups, the subdivisions observed in the parasite tree also fit with many of the subdivisions generally accepted within the Primate order. These results confirm the subgroups previously described in the subfamily and support Cameron's hypothesis in its aspect of association by descent. Although the classification of the Enterobiinae generally closely underlines the classification of Primates, several discordances also are observed. These are discussed case by case, with use of computed reconstruction scenarios. Given that the occurrences of the same pinworm species as a parasite for several congeneric host species is not the generalized pattern, and given that several occurrences also are observed in which the speciations of the parasites describe a more complex network, Cameron's hypothesis of a slower rhythm of speciation in the parasites can be considered partly refuted. The presence of two genera parasitic on squirrels in a family that contains primarily primate parasites also is discussed. The cladistic analysis does not support close relationships between the squirrel parasites and suggests an early separation from the Enterobiinae for the first (Xeroxyuris), and a tardy host-switching from the Platyrrhini to the squirrels for the second (Rodentoxyuris).

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