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Sequences of the primate epsilon-globin gene: implications for systematics of the marmosets and other New World primates.

Sequences of the epsilon-globin gene were determined for five species of marmosets, along with approximately 2 kb of 5' flanking sequence. An analysis of these data, compared with those of other primates strongly supports the classification of Callithrix jacchus and C. geoffroyi into the jacchus group, and C. argentata and C. mauesi into the argentata group. The pygmy marmoset, formerly identified as Cebuella pygmaea joined strongly to the argentata group, indicating that without the pygmy marmoset the genus Callithrix would be paraphyletic. Our data support recent studies which indicate that C. pygmaea should be included in the genus Callithrix. Relationships among other primates were as indicated by previous studies of epsilon-globin sequences. Divergence times were estimated according to a local molecular clock. These calculations indicated the divergence of C. mauesi and C. argentata to be approximately 1.6-1.9 Myr (million years ago), and the most recent common ancestor of the marmosets to be between 4.5 and 4.7 Myr. The latter estimate corresponds well to the date of 4.6 Myr calculated from an independent data set.

Animals↗

Mitochondrial COII gene sequences provide new insights into the phylogeny of marmoset species groups (Callitrichidae, Primates).

Mitochondrial cytochrome oxidase II (COII) gene sequences (549 base pairs) were used to investigate the taxonomic relationships among 12 marmoset (Callithrix, Cebuella and Mico) taxa. A large number of substitutions were found in the third base codon positions, providing a strong phylogenetic signal in a gene coding a conserved protein. Despite the significant affinity between the 2 Amazonian genera Cebuella and Mico, found in recent molecular studies, the analysis presented here did not resolve convincingly the phylogenetic relationships between the 3 genera. Mico nevertheless formed 3 distinct clades, reflecting a basic division of species groups based on geographic distribution (east or west of the Rio Tapajós) rather than morphology (presence or absence of auricular hair). This supports the taxonomic distinction of the allopatric emiliae forms. In Callithrix, Callithrix aurita forms a distinct clade, but the remaining morphotypes form a somewhat contradictory cluster, possibly resulting from an extremely rapid radiation.

Amino Acid Sequence↗

Primate diversity, habitat preferences, and population density estimates in Noel Kempff Mercado National Park, Santa Cruz Department, Bolivia.

This report documents primate communities at two sites within Noel Kempff Mercado National Park in northeastern Santa Cruz Department, Bolivia. Diurnal line transects and incidental observations were employed to survey two field sites, Lago Caiman and Las Gamas, providing information on primate diversity, habitat preferences, relative abundance, and population density. Primate diversity at both sites was not particularly high, with six observed species: Callithrix argentata melanura, Aotus azarae, Cebus apella, Alouatta caraya, A. seniculus, and Ateles paniscus chamek. Cebus showed no significant habitat preferences at Lago Caiman and was also more generalist in use of forest strata, whereas Ateles clearly preferred the upper levels of structurally tall forest. Callithrix argentata melanura was rarely encountered during surveys at Lago Caiman, where it preferred low vine forest. Both species of Alouatta showed restricted habitat use and were sympatric in Igapo forest in the Lago Caiman area. The most abundant primate at both field sites was Ateles, with density estimates reaching 32.1 individuals/km2 in the lowland forest at Lago Caiman, compared to 14.1 individuals/km2 for Cebus. Both Ateles and Cebus were absent from smaller patches of gallery forest at Las Gamas. These densities are compared with estimates from other Neotropical sites. The diversity of habitats and their different floristic composition may account for the numerical dominance of Ateles within the primate communities at both sites.

Alouatta↗

Phylogenetic relationships of the Callitrichinae (Platyrrhini, primates) based on beta2-microglobulin DNA sequences.

The phylogenetic relationships of callitrichine primates have been determined by DNA sequence analyses of exons 1, 2, and 3 of the beta2-microglobulin gene. Parsimony, distance, and maximum likelihood analyses of ca. 900 base pairs of 21 taxa, representing all callitrichine genera, indicated that Saguinus was the most basal offshoot. Within Saguinus, S. fuscicollis appeared as the first divergent lineage followed by an unresolved trichotomy formed by S. mystax/S. imperator, S. midas/S. bicolor, and S. oedipus. A second callitrichine lineage was formed by Leontopithecus; each of the three species studied showed identical nucleotide sequences. Callimico appeared as the sister taxon of Callithrix/Cebuella. Genetic distances within this latter group were very small, although a stronger association between Cebuella and species of the Callithrix argentata group was observed. The inclusion of Cebuella in the genus Callithrix is suggested. These studies indicated that tamarins are more plesiomorphic than marmosets in agreement with the phyletic dwarfism hypothesis.

Animals↗

Variation in circulating and excreted estradiol associated with testicular activity in male marmosets.

Concentrations of estradiol (E2) are high in the urine of male marmosets, and links between E2 and paternal behavior have been proposed in black tufted-ear marmosets, Callithrix kuhlii. However, it is not clear whether urinary E2 in male marmosets: 1) represents production of E2 associated with testicular activity, 2) is associated with adrenal steroid production, or 3) merely reflects peripheral conversion of T to E2 prior to excretion. We tested the hypothesis that urinary E2 in male marmosets represents estrogen production-associated activity in the hypothalamus-pituitary-gonad (HPG) axis. We treated adult male marmosets with gonadotropin-releasing hormone (GnRH), and used saline-treated males as controls. We collected blood and urine samples from males before and after treatment, and assayed them for testosterone (T), estradiol (E2), and cortisol (CORT). Treatment with GnRH increased circulating T and E2, and prevented decreases in levels of urinary T and E2. Moreover, changes in plasma and urinary E2 after treatment were positively correlated with post-treatment changes in T. Thus, our data are consistent with both plasma and urinary E2 in male marmosets increasing as a result of testicular stimulation. However, treatment with GnRH did not affect plasma or urinary CORT concentrations of males, suggesting that the E2 excreted by males is not of adrenal origin. We also compared urinary T, E2, and CORT levels between intact and castrated male common marmosets (Callithrix jacchus). Urinary concentrations of T and E2, but not CORT, were significantly lower in castrated than in intact males, further suggesting that E2 in male marmosets varies with testicular activity.

Animals↗

Systematics and evolution of the Jacchus group of marmosets (Platyrrhini).

Interspecific differentiation and geographic variation patterns in 39 skull traits of eastern Brazilian marmosets are analyzed. Eastern Callithrix taxa are distinct morphologically, and no evidence of intergradation among taxa is observed. Instead, there are sharp, stepped morphological boundaries among taxa, consistent with species-level distinction. The morphological similarity cluster diagram obtained from Mahalanobis distances is different from available molecular trees, and the general picture emerging is that the eastern Callithrix taxa should be considered as good species arising recently in South American history. In particular, C. kuhlii is morphologically distinct from other marmoset taxa, including C. geoffroyi and C. penicillata, which were previously hypothesized to be the parental populations that formed C. kuhlii by hybridization. Furthermore, C. kuhlii populations from southeastern Bahia do not overlap morphologically with any C. penicillata population, including the upper São Francisco River populations that display skin colors and pelage patterns to some extent similar to true Kuhli's marmosets. There is a negative, though insignificant, correlation between the morphological distance matrix and a Mahalanobis distance matrix estimated from nine climatic variables, a pattern opposite to that expected under a parapatric speciation model. This result, together with the lack of clinal variation in skull traits, suggests that an allopatric model of speciation might best explain eastern marmoset diversification.

Analysis of Variance↗

Evolutionary implications of the unusual walking mechanics of the common marmoset (C. jacchus).

Several features that appear to differentiate the walking gaits of most primates from those of most other mammals (the prevalence of diagonal-sequence footfalls, high degrees of humeral protraction, and low forelimb vs. hindlimb peak vertical forces) are believed to have evolved in response to requirements of locomotion on thin arboreal supports by early primates that had developed clawless grasping hands and feet. This putative relationship between anatomy, behavior, and ecology is tested here by examining gait mechanics in the common marmoset (Callithrix jacchus), a primate that has sharp claws and reduced pedal grasping, and that spends much of its time clinging on large trunks. Kinematic and kinetic data were collected on three male Callithrix jacchus as they walked across a force platform attached to the ground or to raised horizontal poles. The vast majority of all walking gaits were lateral-sequence. For all steps, the humerus was retracted (<90 degrees relative to a horizontal axis) or held in a neutral (90 degrees ) position at forelimb touchdown. Peak vertical forces on the forelimb were always higher than those on the hindlimb. These three features of the walking gaits of C. jacchus separate it from any other primate studied (including other callitrichids). The walking gaits of C. jacchus are mechanically more similar to those of small, nonprimate mammals. The results of this study support previous models that suggest that the unusual suite of features that typify the walking gaits of most primates are adaptations to the requirements of locomotion on thin arboreal supports. These data, along with data from other primates and marsupials, suggest that primate postcranial and locomotor characteristics are part of a basal adaptation for walking on thin branches.

Animals↗

Social implications of gummivory in marmosets.

Gummivory or exudate feeding is a major dietary specialization which has received relatively little attention in the literature. While plant exudates contribute to the diet of many primate species, we suggest that the callitrichid species Cebuella pygmaea and Callithrix jacchus are obligate exudate feeders under free-ranging conditions. Callithrix jacchus provides an excellent model for examining the effects of exudate feeding and foraging upon social behavior, since other callitrichid species of similar body size do not share this dietary specialization. We review the effects of exudate foraging on specific social behaviors observed both in field and laboratory populations of C. jacchus. By comparing this species to closely related species, exudate foraging is seen to (1) be retained under laboratory conditions, (2) increase the frequency of territorial marking behavior while decreasing the frequency of overt aggression in males, (3) decrease the duration of infant care, and (4) increase the number of nonadults in social groups but not affect group size. The evidence presented supports the hypothesis that the consequences of exudate foraging in C. jacchus are fundamental and socially complex.

Aggression↗

Relative sizes of cortical visual areas in marmosets: functional and phylogenetic implications.

Visual areas V1, V2 and MT (V5) were identified through myeloarchitectonic criteria and their sizes estimated in a flattened map of caudal cerebral cortex in the marmoset Callithrix penicillata. The ratio MT/V1 in this species is similar to values reported for other species of primates, but the ratio V2/V1 in Callithrix penicillata is smaller than that in macaques and larger than that in Aotus. The possible implications of these results are discussed.

Animals↗

Cross-reactivity of antihuman monoclonal antibodies with cell surface receptors in the common marmoset.

In this report we demonstrate that a large number of monoclonal antibodies (mAbs) against human epitopes cross-react with surface receptors on white blood cells of Callithrix jacchus, indicating species similarities. However, a variety of other mAbs do not exhibit any cross-reactivity, thus also providing evidence for distinct differences in the structure of these receptors among nonhuman primates. Such differences have to be known and taken into consideration when attempting extrapolations between species. The results presented provide the prerequisite for performing extensive studies on immunological structures and functions in marmosets under normal and pathological conditions. We conclude that the immune system of Callithrix jacchus is a convenient model for studies on immunotoxicity with relevance for man, and for this purpose it is clearly superior to that of any rodent species.

Animals↗

Studies on the immunoglobulin-E system of the common marmoset in comparison with human data.

In the common marmoset (Callithrix jacchus jacchus) immunoglobulin E (IgE) serum levels and IgE synthesis of peripheral blood mononuclear cells (PBMC) in vitro were investigated in order to look for homologies to the human system. While IgE was not found in marmoset blood plasma with three commercial antihuman IgE-kits with monoclonal antibodies (mAbs), two other kits using polyclonal antibodies against human IgE revealed detectable IgE concentrations of up to 10 kU/liter in plasma samples of 19 out of 21 marmosets. In accord with human data, rhIL-4 showed biological functions under in vitro conditions in PBMC of the New World monkey. Proliferation, measured by 3H-thymidine incorporation, of isolated PBMC of marmosets could be induced by rhIL-4. FACScan analysis showed an enhanced expression of the low affinity IgE receptor CD23 (Fc epsilon RII) on CD20+ B lymphocytes after incubation with rhIL-4. Furthermore, PBMC from marmosets could be stimulated by IL-4 alone or in combination with dexamethasone as well as with lipopolysaccharide (E. coli) to produce IgE in culture. The results indicate that Callithrix jacchus is using an IgE system that is rather similar to that of humans, although not completely identical. Antihuman mAbs and rhIL-4 can be used to investigate IgE regulation in vitro of marmoset PBMC. These data encourage the development of a primate animal model for studying possible modifications of the IgE system under pathological conditions to find new therapeutic strategies in atopic diseases.

Animals↗

Polymorphism of visual pigments in a callitrichid monkey.

Microspectrophotometric measurements of visual pigments have been obtained for a large sample of New World monkeys of the species Callithrix jacchus jacchus. These animals exhibit a polymorphism of visual pigments. The rods (Lmax 499 nm) and the short-wave receptors (Lmax 423 nm) appear to be common to all animals but individuals differ in the number and spectral position of pigments in the green-yellow spectral region. The latter pigments cluster near 545, 559 and 567 nm. Male monkeys draw one pigment from this set and female monkeys may draw one or two. The results are generally consistent with a genetic theory that postulates in Callithrix three possible alleles for a single locus in the X-chromosome. It appears that polymorphisms of cone pigments may be widespread among neotropical primates.

Animals↗

Toxoplasmosis in a colony of New World monkeys.

In a colony of New World monkeys five tamarins (Saguinus oedipus, Saguinus labiatus and Leontopithecus rosal. rosal.), three marmosets (Callithrix jacchus and Callithrix pygmaea) and one saki (Pithecia pithecia) died suddenly. The colony comprised 16 marmosets, 10 tamarins and three sakis. The main pathological findings were necrotic lesions in the lung, the intestine, and the liver. Histopathologically T. gondii parasites were observed in organs from the tamarins and the marmosets but not in the saki. Some considerations on epidemiology are presented. Preventive measures were directed against the bottom layer of the cages, on cockroach extermination, and on freezing of raw meat.

Animal Feed↗

Molecular mass and isoelectric properties of pituitary and urinary gonadotrophins in callitrichid primates.

In this study, the molecular masses and isoelectric characteristics of pituitary LH and FSH in two species of callitrichid primate, the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus), were determined. Comparative data for urine samples from Callithrix jacchus are also presented. The separation of gonadotrophins from pituitary extracts and urine was performed under nonreducing conditions using SDS-PAGE and isoelectric focusing procedures. Hormone activity in gel eluates was determined by in vitro bioassays for LH and FSH and by a microtitre plate enzymeimmunoassay for LH. The molecular masses of pituitary and urinary proteins were between 36 and 37 kDa for LH and FSH, and were similar in both species. A dimer form of pituitary LH with a molecular mass of 33 kDa was also found in the cotton-top tamarin, but not in the marmoset. Guanidine-HCl dissociation of gonadotrophins from marmoset and tamarin pituitaries before electrophoresis gave proteins of 16 and 28 kDa, and 16 and 25 kDa range, respectively. Isoelectric focusing revealed numerous peaks of bioactivity for both LH and FSH, indicating the presence of multiple molecular variants (isoforms) of each hormone. In both species pituitary FSH eluted over a narrower and more acidic pH range than LH. Isoelectric focusing profiles for pituitary and urinary LH in the marmoset were similar (pH range 5.0-8.5), whereas urinary FSH demonstrated a more acidic profile than the pituitary protein. These results give comparative information on the properties of New World primate gonadotrophins, which should be useful in studies of their physiological action and in aiding the development of improved reagents and assays for their detection.

Animals↗

Developmental biology of the common marmoset: proposal for a "postnatal staging".

The published knowledge on neurobiological, psychological, and ethological aspects of development in Callithrix jacchus is still limited. We have collected published and unpublished data from several Callithrix colonies and pooled information on criteria for developmental progress and maturation using a questionnaire sent to numerous experts in the field. The data suggest that developmental stages can be defined not only for the embryonic and fetal but also for the postnatal period. Based on multifactorial definitions, using criteria selected from maturational changes in the motor and visual systems and behavioral features, we propose to subdivide postnatal development of the common marmoset into seven periods ("stages").

Animals↗

Gelatin as a vehicle for food and vitamin administration to marmosets.

For a period of three years, gelatin was used as a vehicle for administration of food, vitamin complex and drugs to laboratory maintained Callithrix penicillata and Callithrix jacchus marmosets and a breeding colony of C. penicillata. In both circumstances, results were satisfactory. The animals survived for long periods of time, with adult, young and juvenile primates in the breeding colony showing good physical condition.

Animal Feed↗

Nasal and intrathalamic inoculations of primates with Tacaribe virus: protection against Argentine hemorrhagic fever and absence of neurovirulence.

Callithrix jacchus marmosets were inoculated by different routes with two stocks of Tacaribe virus, one from suckling mouse brain and another from human diploid MRC5 cells. All 12 primates inoculated by nasal route developed neutralizing serum antibodies without any clinical signs. All 6 primates receiving the mouse brain-Tacaribe virus were protected against lethal challenge with pathogenic XJ strain of Junin virus, while protection was also conferred in 4 out of 6 primates receiving the diploid cell-Tacaribe virus stock. Intramuscular (i.m.) inoculation also elicited antibodies and conferred protection to 4 primates receiving the diploid cell-virus stock. Intrathalamic (i.t.) inoculation of mouse brain-virus stock caused no clinical signs or histopathologic changes in groups of 3 primates each examined on days 33 and 90 post-infection (p.i.). All primates developed antibody response, but no virus could be detected in their brain. Thus, Tacaribe virus proved harmless and immunogenic in Callithrix jacchus and protected most marmosets against challenge with the lethal XJ strain of Junin virus.

Administration, Intranasal↗

Reproductive performance of three species of Callitrichidae.

The reproductive performance of three species of Callitrichidae housed under identical conditions, including relatively spacious caging and visual screening, was compared. The three species were Callithrix jacchus, Saguinus fuscicollis, and Saguinus oedipus. Callithrix jacchus was the most reliable breeder, with the lowest percentage of stillborn and the highest post-weaning survival. While the reproductive performance of S oedipus was better than that generally reported for other colonies, the reproductive performance of the Saguinus species was still poorer than that of C jacchus. The two Saguinus species did not differ significantly in either percentage of stillborn or post-weaning survival. None of the species showed infertility due to lactation, but the mean inter-birth interval was significantly longer for S oedipus than for either C jacchus or S fuscicollis.

Animals↗