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The use of vocal signals in the social play of barbary macaques.

Field studies in various species of Macaca (Cercopithecidae) provided evidence for specific visual displays that typically accompany playful interactions. The aim of our study was to examine whether and when playing individuals would use auditory displays, i.e. vocalizations that often occur during social play as well. The study was conducted on a population of semi-free Barbary macaques (Macaca sylvanus) with a special focus on the composition and dynamics of playful wrestling (synonymous term: 'rough-and-tumble play'). Analyses of dyadic encounters between subadult males allowed us to distinguish five types of playful behaviours and three types of vocalizations. The latter were clearly linked to encounters where effects of visual signals were impaired, e.g. during close body contact. During wrestling, vocalizations tended to increase in the beginning of an encounter, whereas the last seconds of wrestling often showed a decline in vocalization rate. Our results allowed us to conclude that these vocalizations may supplement or in many cases even substitute interactional effects of visual signals, e.g. the 'play face.'

Animals↗

Phylogenetic analysis of the Friedreich ataxia GAA trinucleotide repeat.

Friedreich ataxia is an autosomal recessive neurodegenerative disorder associated with a GAA repeat expansion in the first intron of the gene (FRDA) encoding a novel, highly conserved, 210 amino acid protein known as frataxin. Normal variation in repeat size was determined by analysis of more than 600 DNA samples from seven human populations. This analysis showed that the most frequent allele had nine GAA repeats, and no alleles with fewer than five GAA repeats were found. The European and Syrian populations had the highest percentage of alleles with 10 or more GAA repeats, while the Papua New Guinea population did not have any alleles carrying more than 10 GAA repeats. The distributions of repeat sizes in the European, Syrian, and African American populations were significantly different from those in the Asian and Papua New Guinea populations (p < 0.001). The GAA repeat size was also determined in five nonhuman primates. Samples from 10 chimpanzees, 3 orangutans, 1 gorilla, 1 rhesus macaque, 1 mangabey, and 1 tamarin were analyzed. Among those primates belonging to the Pongidae family, the chimpanzees were found to carry three or four GAA repeats, the orangutans had four or five GAA repeats, and the gorilla carried three GAA repeats. In primates belonging to the Cercopithecidae family, three GAA repeats were found in the mangabey and two in the rhesus macaque. However, an AluY subfamily member inserted in the poly(A) tract preceding the GAA repeat region in the rhesus macaque, making the amplified sequence approximately 300 bp longer. The GAA repeat was also found in the tamarin, suggesting that it arose at least 40 million years ago and remained relatively small throughout the majority of primate evolution, with a punctuated expansion in the human genome.

Alleles↗

Distribution of intrachromosomal telomeric sequences (ITS) on Macaca fascicularis (Primates) chromosomes and their implication for chromosome evolution.

The intrachromosomal location of the telomeric sequence in the crab-eating macaque, Macaca fascicularis (F. Cercopithecidae, Catarrhini) has been analysed by fluorescent in situ hybridisation with a long synthetic (TTAGGG)(n) probe. A total of 237 metaphases was analysed. As expected, all telomeres hybridised with the probe and 90 intrachromosomal loci with different hybridisation frequencies were also detected. The chromosomal location of interstitial telomeric sequences in M. fascicularis and in Homo sapiens was then compared, 37 sites (41.11%) being found to be conserved. Some of these sequences can be derived from rearrangements, such as inversions (MFA13q23) or fusions (MFA2p13 and MFA13p12), that have taken place during karyotype evolution.

Animals↗

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↗

Khat (Catha edulis) up-regulates testosterone and decreases prolactin and cortisol levels in the baboon.

The potential effect of Khat (Catha edulis, Celastraceae) on fertility in humans has not been elucidated. In this study, we used the olive baboon (Papio anubis, Cercopithecidae) to determine the effects of oral administration of khat on circulating hormones. In order to establish baseline hormonal levels, five male baboons were bled once a week for 1 month. The same baboons were then fed with crude khat juice extract once a week over a period of 2 months, and the effects on serum levels of cortisol, testosterone and prolactin determined using enzyme immunoassay (EIA) and radioimmunoassay (RIA). Subsequently, sampling was repeated for a further 1 month to determine the residual effect of khat. The results showed that khat administration causes a significant increase in the mean levels of testosterone while prolactin and cortisol levels were reduced. These effects were also evident 1 month post treatment and indicate khat may exert a transient effect on male fertility by interfering with the hormonal profiles.

Administration, Oral↗

Fig-eating by vertebrate frugivores: a global review.

The consumption of figs (the fruit of Ficus spp.: Moraceae) by vertebrates is reviewed using data from the literature, unpublished accounts and new field data from Borneo and Hong Kong. Records of frugivory from over 75 countries are presented for 260 Ficus species (approximately 30% of described species). Explanations are presented for geographical and taxonomic gaps in the otherwise extensive literature. In addition to a small number of reptiles and fishes, 1274 bird and mammal species in 523 genera and 92 families are known to eat figs. In terms of the number of species and genera of fig-eaters and the number of fig species eaten we identify the avian families interacting most with Ficus to be Columbidae, Psittacidae, Pycnonotidae, Bucerotidae, Sturnidae and Lybiidae. Among mammals, the major fig-eating families are Pteropodidae, Cercopithecidae, Sciuridae, Phyllostomidae and Cebidae. We assess the role these and other frugivores play in Ficus seed dispersal and identify fig-specialists. In most, but not all, cases fig specialists provide effective seed dispersal services to the Ficus species on which they feed. The diversity of fig-eaters is explained with respect to fig design and nutrient content, phenology of fig ripening and the diversity of fig presentation. Whilst at a gross level there exists considerable overlap between birds, arboreal mammals and fruit bats with regard to the fig species they consume, closer analysis, based on evidence from across the tropics, suggests that discrete guilds of Ficus species differentially attract subsets of sympatric frugivore communities. This dispersal guild structure is determined by interspecific differences in fig design and presentation. Throughout our examination of the fig-frugivore interaction we consider phylogenetic factors and make comparisons between large-scale biogeographical regions. Our dataset supports previous claims that Ficus is the most important plant genus for tropical frugivores. We explore the concept of figs as keystone resources and suggest criteria for future investigations of their dietary importance. Finally, fully referenced lists of frugivores recorded at each Ficus species and of Ficus species in the diet of each frugivore are presented as online appendices. In situations where ecological information is incomplete or its retrieval is impractical, this valuable resource will assist conservationists in evaluating the role of figs or their frugivores in tropical forest sites.

Animals↗

Origin of human chromosome 21 and its consequences: a 50-million-year-old story.

Great apes (Pongidae) possess a chromosome similar to human chromosome 21 (HSA21), whose trisomy was described in both chimpanzee and orangutan. Having studied more than 200 mammalian species by chromosome banding techniques and reconstructed Primates phylogeny, we reinvestigated, using fluorescence in situ hybridization, primate and non-primate mammals that we considered to possess a karyotype representative of their taxonomic group. DNA sequences from HSA21 and human chromosome 3 (HSA3) are synthenic and form a large and similar chromosome in species from distinct orders, such as Primates, Carnivora, Artiodactyla and Scandentia. In Primates, this syntheny was maintained in lemurs and was disrupted by a fission in Old World monkeys (catarrhines). Another fission occurred in New World monkeys (platyrrhines), conserving a syntheny between HSA21 and a very short segment of HSA3 DNA sequences. Thus, the ancestral HSA21 was formed after the divergence between platyrrhines and catarrhines and before the emergence of Cercopithecidae. This exposed the human and Pongidae ancestry to trisomy 21 for a period of 30-50 million years, while, in other catarrhines, the equivalent of HSA21 was further involved in various translocations forming large chromosomes whose aneuploidy, very probably incompatible with life, protected them against trisomy 21.

Aneuploidy↗

Fragile sites in human and Macaca fascicularis chromosomes are breakpoints in chromosome evolution.

We have analysed the expression of aphidicolin-induced common fragile sites at two different aphidicolin concentrations (0.1 micromol/L and 0.2 micromol/L) in three female and one male crab-eating macaques (Macaca fascicularis, Cercopithecidae, Catarrhini). A total of 3948 metaphases were analysed: 1754 in cultures exposed to 0.1 micromol/L aphidicolin, 1261 in cultures exposed to 0.2 micromol/L aphidicolin and 933 in controls. The number of breaks and gaps detected ranged from 439 in cultures exposed to 0.1 micromol/L aphidicolin to 2061 in cultures exposed to 0.2 micromol/L aphidicolin. The use of a multinomial FSM statistical model allowed us to identify 95 fragile sites in the chromosomes of M. fascicularis, of which only 16 are expressed in all four specimens. A comparative study between the chromosomes of M. fascicularis and man has demonstrated that 38 human common fragile sites (50%) are found in the equivalent location in M. fascicularis. The analysis of the rearrangements that have taken place during chromosome evolution has revealed that the breakpoints involved in these rearrangements correspond significantly (p < 0.025) to the location of M. fascicularis fragile sites.

Animals↗

Rhesus monkey model for Leishmania major transmitted by Phlebotomus papatasi sandfly bites.

Leishmaniasis research needs a near-human model for investigations of natural infection processes, immunological responses and evaluation of treatments. Therefore, we developed a reproducible system using Leishmania major Yakimoff & Schokhor (Trypanosomatidae: Kinetoplastida), the cause of Old World zoonotic cutaneous leishmaniasis (ZCL), transmitted to rhesus monkeys Macaca mulatta (Zimmerman) (Primates: Cercopithecidae) by sandfly bites of experimentally infected Phlebotomus papatasi (Scopoli) (Diptera: Psychodidae). Eight monkeys of presumed Indian origin (Leishmania naive) were exposed to bites of female sandflies that had been infected with L. major by membrane-feeding on human blood seeded with amastigotes isolated from hamster footpad lesions. Infection rates of membrane-fed sandflies averaged > 85% seven days after the infective feed, with uniformly high numbers of promastigotes in the stomodaeal valve region of the sandfly gut. Nodules and ulcerating dermal lesions developed on 7/8 monkeys 2-4 weeks post-bite and persisted for 3-7 months. Monkeys also developed satellite lesions beyond the area of sandfly bites on the head, but not on the chest. Three re-challenged monkeys developed lesions that healed faster than lesions from their primary challenges. After infection, monkeys developed delayed type hypersensitivity (DTH) responses to a panel of Leishmania skin test antigens (LSTA) and, when tested by ELISA and IFA, showed significant post-infection antibody titres which typically rose for approximately 170 days and then gradually receded during the next 100 days following the first challenge. After the second challenge, antibody titres spiked higher within approximately 50 days and receded more rapidly. In contrast, four rhesus macaques of Chinese origin developed no lesions following infected sandfly bites, although they raised antibodies and LSTA reactions, indicating subclinical infection.

Animals↗

Occurrence of hepatitis viruses in wild-born non-human primates: a 3 year (1998-2001) epidemiological survey in Gabon.

Hepatitis B and C infections are endemic in human population in central Africa, particularly in Gabon. The aim of this study was to determine the prevalence of hepatitis B virus (HBV) and eventual occurrence of hepatitis C virus (HBC)-related strains in a variety of wild-born non-human primates living in Gabon and Congo. Plasma samples were screened for HBV and HCV markers. A non-invasive method of DNA extraction from faeces followed by specific HBV-DNA amplification was developed to study this infection in wild troops of chimpanzees and gorillas. No HCV infection in non-human primates, wild-born or captive, was detected among 596 samples tested. No HBV infection could be detected in samples tested and obtained from Cercopithecidae. In contrast, 14.7 and 42.2% of wild-born chimpanzees in Gabon and Congo were infected with HBV or had evidence of past HBV infection. At Centre International de Recherches Médicales (CIRMF) Primate Centre, 32.1% of chimpanzees and gorillas were HBV positive or had evidence of past infection. In the cases with past infection, 5.9% wild-born and 8.3% at CIRMF harboured HBV-DNA despite the presence of neutralizing HbsAb. Together with previous findings, we confirm the high HBV prevalence not only in humans but also in chimpanzees and gorillas in Gabon and Congo.

Animals↗

Evolution of the primate cathelicidin. Correlation between structural variations and antimicrobial activity.

Cathelicidin genes homologous to the human CAMP gene, coding for the host defense peptide LL-37, have been sequenced and analyzed in 20 primate species, including Great Apes, hylobatidae, cercopithecidae, callithricidae, and cebidae. The region corresponding to the putative mature antimicrobial peptide is subject to a strong selective pressure for variation, with evidence for positive selection throughout the phylogenetic tree relating the peptides, which favors alterations in the charge while little affecting overall hydrophobicity or amphipathicity. Selected peptides were chemically synthesized and characterized, and two distinct types of behavior were observed. Macaque and leaf-eating monkey RL-37 peptides, like other helical antimicrobial peptides found in insect, frog, and mammalian species, were unstructured in bulk solution and had a potent, salt and medium independent antimicrobial activity in vitro, which may be the principal function also in vivo. Human LL-37 and the orangutan, hylobates, and callithrix homologues instead showed a salt-dependent structuring and likely aggregation in bulk solution that affected antimicrobial activity and its medium dependence. The two types of peptides differ also in their interaction with host cells. The evolution of these peptides has thus resulted in distinct mechanisms of action that affect the direct antimicrobial activity and may also modulate accessory antimicrobial functions due to interactions with host cells.

Amino Acid Sequence↗

First description of a new species of Demodex (Acari: Demodecidae) from rhesus monkey.

Species of Demodex live in hair follicles and sebaceous glands of many species of mammals. Demodex macaci n .sp. is described (all life stages) from a captive rhesus monkey, Macaca mulatta (Zimmermann, 1780). Mites were found at all levels of the hair follicles and occasionally in sebaceous glands of the skin of the perineal region. This is the first description of a demodectic hair follicle mite from the primate family Cercopithecidae.

Animals↗

Macroevolutionary inferences from primate phylogeny.

We apply new statistical methods to a recent estimate of the phylogeny of all living primate species to test a range of models of cladogenesis. Null models in which probabilities of speciation and extinction do not differ among contemporaneous lineages are not consistent with the phylogeny. We present evidence that the net rate of cladogenesis (speciation rate minus extinction rate) increased in the lineage leading to the Cercopithecidae (Old World monkeys), and that there have been further increases in some lineages within that family. Such increases suggest the occurrence of clade selection, although we have not identified the selected trait or traits. There is no evidence that the net rate of cladogenesis is a function either of how many primate lineages are already present or of time. Intriguingly, three other clades--Strepsirhini, Platyrrhini and Hominoidea--appear to have had very similar rates of clade growth, in spite of their great biological differences.

Animals↗

Evolution of pro-protamine P2 genes in primates.

Protamines P1 and P2 form a family of small basic peptides that represent the major sperm proteins in placental mammals. In human and mouse protamine P2 is one of the most abundant sperm proteins. The protamine P2 gene codes for a P2 precursor, pro-P2 which is later processed by proteolytic cleavages in its N-terminal region to form the mature P2 protamines. We have used polymerase chain amplification to directly sequence the pro-P2 genes of the five major primate families: red howler (Alouatta seniculus) is a New World monkey (Cebidae); the two macaque species, Macaca mulatta and M. nemistrina are Old World monkeys (Cercopithecidae), the gibbon, Hylobates lar, represents one branch of the apes (Hylobatidae); the orangutan, Pongo pygmaeus, gorilla, Gorilla gorilla and two species of chimpanzee Pan paniscus and Pan troglodytes represent a second ape family (Pongidae). These pro-P2 genes are compared with that of human [Domenjoud, L., Nussbaum, G., Adham, I. M., Greeske, G. & Engel, W. (1990) Genomics 8, 127-133]. The overall size and organization of the genes are conserved within the group. The mean length of pro-P2 is 101 residues, with an increase to 102 in M. nemistrina and a decrease to 99 residues in red howler (A. seniculus). In gorilla and red howler one of two 79-bp tandem repeats that occurs 3' of the gene is deleted. Of the 101 deduced amino acids examined, an amino acid change occurs in one or more primates at 45 positions. Considering only the most recently diverged group, the human/gorilla/chimpanzee clade, this represents a very high mutation rate of 0.99 changes/100 sites in 10(6) years. This rapid mutation rate is characteristic of both members of the protamine gene family, P1 and P2. Consideration of the variable nature of the sequences at the multiple sites of proteolysis during the processing of the pro-P2 indicates either that there are several processing enzymes of differing specificities, or more likely that the folded structure of the pro-P2 limits accessibility of a non-specific protease to certain exposed sites.

Alouatta↗

Intestinal parasitism--protozoa and helminths--in primates at the Barcelona Zoo.

The faunistic results regarding intestinal parasitism by protozoa and helminths in 21 primate species (three Cebidae, thirteen Cercopithecidae, one Hylobatidae, one Lemuridae, three Pongidae) are reported. The primate species were housed in four separate galleries. Six faecal samples of each host species were subjected to coprological analysis. Fifteen parasite species were detected: 11 protozoa (Entamoeba coli, E. chattoni, E. hartmanni, Iodamoeba bütschlii, Endolimax nana, Giardia intestinalis, Chilomastix mesnilii, Enteromonas hominis, Trichomonas intestinalis, Balantidium coli, and Blastocystis hominis) and 4 helminths (Ancylostoma sp., Strongyloides fuelleborni, Strongyloides sp., and Trichuris trichiura). The results reveal certain parasitic similarities between host species housed in the same gallery; however, these primate species do not always carry identical parasite species.

Animals↗

Taste preference in nonhuman primates to compounds sweet in man.

Primates have stimulated more interest than any other group as humans are ranked in this same mammalian order. Gustatory responses of human and nonhuman primates have already been compared for compounds such as monosaccharides, oligosaccharides, polyols, amino acids, dipeptides, proteins, dihydrochalcones, sulfamates, saccharin, acesulfame, diterpenes or urea derivatives, all known to be sweet in man. But no rational comparison in primates has been attempted. Using a structure-activity relationship study in primates, it is now possible to classify the primate sweetness receptors into four types according to the behavioral responses observed from various selected compounds sweet in humans. The four types are represented by (1) the Callitrichidae and (2) the Cebidae, both from the infraorder Platyrrhini (New World monkeys), (3) the Lemuridae and Lorisidae, from the suborder Prosimii (prosimians), and (4) the Cercopithecidae (Old World monkeys), Hylobatidae (lesser apes), Pongidae (great apes), and Hominidae (humans) from the infraorder Catarrhini (Old World simians). By a comparative study of the putative receptor recognition sites postulated for each type of receptor, it is inferred that the Callitrichidae (marmosets and tamarins) have retained the most primitive sweetness receptor among primates. As we believe that the evolution of the sweetness receptor is a key factor involved in the raising of nonhuman primates from a 'primitive grade' towards a more 'advanced' or 'simian grade,' the possible phylogenetic implications of these findings will be discussed.

Animals↗

Effects of positively selected sequence variations in human and Macaca fascicularis beta-defensins 2 on antimicrobial activity.

The evolution of orthologous genes coding for beta-defensin 2 (BD2) in primates has been subject to positive selection during the divergence of the platyrrhines from the catarrhines and of the Cercopithecidae from the Hylobatidae, great apes, and humans. Three peptides have been selected for a functional analysis of the effects of sequence variations on the direct antimicrobial activity: human BD2 (hBD2), Macaca fascicularis BD2 (mfaBD2), and a variant of the human peptide lacking Asp(4), (-D)hBD2, which is characteristic only of the human/great ape peptides. hBD2 and mfaBD2 showed a significant difference in specificity, the former being more active towards Escherichia coli and the later towards Staphylococcus aureus and Candida albicans. Asp(4) in the human peptide appears to be important, as (-D)hBD2 was less structured and had a markedly lower antimicrobial activity. The evolution of beta-defensin 2 in primates may thus have been driven, at least in part, by different environmental pressures so as to modulate antimicrobial activity.

Amino Acid Sequence↗

Baboon/human homologies examined by spectral karyotyping (SKY): a visual comparison.

Baboon (Papio hamadryas) metaphase chromosomes were analyzed using spectral karyotyping (SKY), a technique combining fluorescence microscopy, CCD-imaging, and Fourier spectroscopy. Results from a comparison of SKY analyses using probes derived from human chromosomes on baboon metaphases were consistent with the majority of comparative gene mapping data between the two species. These data were also compatible with earlier studies comparing macaque and human chromosomes. Human (HSA) chromosome 2 was homologous to baboon (PHA) chromosomes 12 (HSA 2q) and 13 (HSA 2p), whereas three baboon chromosomes corresponded to two different human chromosomes: PHA 3 to HSA 7 and HSA 21, PHA 7 to HSA 14 and HSA 15, and PHA 10 to HSA 20 and HSA 22. These results support the retained synteny between the Hominidae and Cercopithecidae genomes.

Animals↗