Karyotypic evolution in Aotus

Great karyotypic diversity exists within the platyrrhine genus Aotus. Primarily by comparing banded karyograms of different forms of Aotus, the pattern of karyotypic evolution can be assessed. Out-group comparisons are used to establish primitive and derived states of particular chromosomes, and a parsimonious cladogram is constructed. Other karyotypic changes are then positioned at appropriate nodes of the cladogram. The resulting phylogenetic hypothesis is entirely self-consistent, is in accord with out-group comparisons, does not invoke hybridization between ancestral forms, and, importantly, indicates a single origin for each rearrangement of euchromatic segments. Moreover, it is consistent with the hypothesis, derived from pelage studies, that the more southerly Aotus taxa constitute a holophyletic group. The reconstructed ancestral karyotype had a diploid number of 54. There has been little loss of euchromatic material during Aotus evolution.     

Chromosome evolution in the owl monkey,Aotus

We have reported nine distinct karyotypes for Aotus, of four pelagic phenotypes, and suggest that this single species has undergone extensive subspeciation. We reconstruct the mechanism of chromosomal evolution and propose a hypothesis about the events of subspeciation in Aotus. We speculate that isolated groups of ancestral individuals living in several confined areas have separately accumulated a fusion or inversion pair as a result of inbreeding. A subsequent reassociation of descendants from these individuals led to the formation of offspring with mixtures of fusion or inversion pairs in their complements. They, in turn, radiated into different ecological niches accompanied by adaptive genetic changes and eventually gave rise to the present forms of Aotus distinguishable by their karyotypes, but not easily recognizable by ordinary taxonomic criteria.     

Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon lowlands of Peru

In the Amazon lowlands of Peru, Aotus nancymai and A. vociferans were observed to use four different types of sleeping sites: (1) holes in the trunks and branches of dry or senescent trees; (2) concavities in polyaxial branching nodes of trees protected by dense entanglements of creepers, climbing plants, vines, and masses of diverse epiphytes; (3) complex sites among masses of epiphytes, climbers, and vines; and (4) simple sites among thickets and dense foliage. Each type is described. There was competition and sharing of sleeping holes between Aotus and other nocturnal arboreal mammals.     

Aotus vociferans ×Aotus nancymai: Sympatry without chromosomal hybridation

In a study relating geographic distribution ofAotus populations with karyotype and coat pattern,Hershkovitz (1983) suggested that this genus comprises nine species.A. vociferans (2n=46) is distributed along the left bank of the Maranon river, andA. nancymai (2n=54) along the right bank of the same river. In the present study we analyzed the karyotypes of 11A. vociferans and 11A. nancymai specimens using G- and C-banding and NOR-staining. Of these animals, fiveA. vociferans were sympatric with fiveA. nancymai in Isla Aramaza, Colombia; oneA. vociferans was sympatric with threeA. nancymai in Yahuma, Peru; oneA. vociferans was sympatric with threeA. nancymai in Terezinha I, Brazil. No signs of hybridation between the taxa was observed at any time, with allA. vociferans having 2n=46 and allA. nancymai 2n=54, as previously reported in the literature. These data suggest thatA. vociferans andA. nancymai should indeed be distinct species.     

Plasmodium vivax under the microscope: the Aotus model

The Aotus model for vivax malaria is extremely useful both as a source of living parasites in non-endemic areas, and as a model for vaccine and drug development research. Several species of New World primates can be infected with numerous different strains of Plasmodium vivax. This article reviews some aspects of the Aotus model, discusses the frequently observed hematological changes that can confound interpretation of hemogram data during the course of vivax infection, and provides a partial atlas of parasite forms and Aotus nancymai blood cells.     

Two new karyotypes in the Peruvian owl monkey (Aotus trivirgatus)

The observation of remarkable karyotypic variation in owl monkeys (Aotus trivirgatus) stimulated us to study the chromosomal evolution of this New World genus. As an extension of this project, we examined the chromosome complement of a “phenotype-B” Aotus population from Peru. In addition to karyotype V(2n = 46), two new karyotypes with diploid numbers of 47 and 48 were identified. A G-band comparison of these karyotypes indicated that the chromosome number polymorphism in these Peruvian owl monkeys resulted from a single fusion or fission event involving a single metacentric and two acrocentric chromosome pairs. This mechanism is also known to be responsible for the chromosome number polymorphism in at least two other populations of phenotype B Aotus, one from Colombia and the other from Panama.     

Population densities and geographic distribution of night monkeys (Aotus nancymai and Aotus vociferans) (cebidae: Primates) in Northeastern Peru

Population densities of two species of night (or owl) monkeys (Aotus nancymai and Aotus vociferans) were estimated using transect census methods. Densities of Aotus nancymai were approximately 46.3 individuals/km² in lowland forests and 24.2 individuals/km² in highland forests. For Aotus vociferans densities were 33.0 individuals/km² in lowland forests and 7.9 individuals/km² in highland forests. A. vociferans occurs north of the Río Amazonas-Marañon and A. nancymai south of it, except for the northern enclave between the Ríos Tigre and Pastaza. The two species are nowhere sympatric. However, the two known karyotypic forms of A. vociferans occupy the same habitats throughout the Peruvian range of the species.     

Identification,classification and evolution of Owl Monkeys (<Emphasis Type="Italic">Aotus</Emphasis>, Illiger 1811)

Background  

Owl monkeys, belonging to the genus Aotus, have been extensively used as animal models in biomedical research but few reports have focused on the taxonomy and phylogeography of this genus. Moreover, the morphological similarity of several Aotus species has led to frequent misidentifications, mainly at the boundaries of their distribution. In this study, sequence data from five mitochondrial regions and the nuclear, Y-linked, SRY gene were used for species identification and phylogenetic reconstructions using well characterized specimens of Aotus nancymaae, A. vociferans, A. lemurinus, A. griseimembra, A. trivirgatus, A. nigriceps, A. azarae boliviensis and A. infulatus.     

Erythrocyte glyoxalase I polymorphism in the owl monkey,Aotus

Three erythrocyte glyoxalase I phenotypes were observed in a sample of 235 karyotypically defined New World owl monkeys, Aotus. The selective distribution of glyoxalase I allele (GLO¹, GLO²) is related to the karyotype of each animal. Owl monkeys with a karyotype VI had an equal distribution of GLO¹ and GLO² genes in the population. Aotus with karyotype II, III, IV, or V had, exclusively, the GLO² allele (expressed as the fast electrophoretic phenotype), in contrast with monkeys with karyotype I or VII, which had only the GLO¹ allele (expressed as the slow electrophoretic phenotype).     

Cytogenetic studies of Aotus from Eastern Amazonia. Y/Autosome rearrangement

Twenty-one specimens of Aotus were captured on both sides of the Tocantins river when the hydroelectric reservoir of Tucuruí, Brazil, was filled. The males had a diploid number of 49 chromosomes, and the females had 50. The observed difference is a consequence of the fusion of the Y chromosome with an autosome. The karyotype is similar to that of the Bolivian Aotus (A. azarae boliviensis). It differs, however, in the G- and C-banding patterns of the chromosome resulting from the Y/autosome fusion. The nucleolar organizing region is located on the secondary constriction of a pair of submetacentric chromosomes. Considerations are presented on the classification of A. infulatus as a separate species.     

Molecular Phylogenetics of <Emphasis Type="Italic">Aotus</Emphasis> (Platyrrhini,Cebidae)

The accurate identification of taxa of Aotus is essential for 1) the development of precise biomedical assays, 2) the determination of potential illegal traffic of this genus, and 3) conservation. Although many studies have contributed to what we know about the phylogenetics of Aotus, none used a sufficiently large number of samples to clarify its complexity. To address this need, we sequenced 696 base pairs of the mitochondrial cytochrome-oxidase II gene (mtCOII) in 69 specimens of 7 taxa of Aotus. We also analyzed 8 microsatellite loci in 136 individuals of 6 taxa. In contrast to previous studies, we sampled only wild individuals and have a precise geographical origin for each one. The mtDNA results showed that: 1) the northern gray-necked group of Aotus is genetically more homogeneous than the polyphyletic red-necked group of Aotus; 2) the ancestors of Aotus vociferans seem to be the original species candidate for the current Aotus; 3) Aotus azarae azarae and A. a. boliviensis are the most differentiated taxa, likely a result of extreme genetic drift during stasipatric speciation; 4) the first genetic splits found among taxa of Aotus occurred during the Pliocene (or even Miocene) while the most recent ones happened during the Pleistocene, when forest refugia may have played an important role in speciation. The mean number of microsatellite alleles was 3–5.33 alleles per locus. We found some private alleles that could be useful in helping to identify illegal trade, although a larger sample size is needed to ensure that these alleles are really private to the relevant taxa. These new findings increase our understanding of the phylogeny of Aotus and the level of genetic diversity within different taxa of Aotus.     

Owl monkeys (Aotus) are highly divergent in mitochondrial Cytochromec Oxidase (COII) sequences

The evolutionary history and differentiation of the owl or night monkeys (Aotus),remain poorly resolved. Variation in pelage and skeletal morphology is relatively minor across their broad range, but cytogenetic studies have revealed that at least 12 karyotypically distinct forms exist, with 2Nchromosome numbers ranging from 46 to 58. We obtained DNA samples from three putative species- A. lemurinus, A. nancymae,and A. azarae-and five karyotypes (I, II, III, IV and VI), amplified the mitochondrial cytochrome coxidase subunit II gene (COII) via PCR and sequenced it. Comparisons of the sequences indicate relatively high levels of sequence divergence among the putative species (4.3 to 6.3%), and suggest that the taxa are genetically quite distinct and have likely experienced extended periods of isolated evolution. The levels of COII divergence represent approximately one- third of the levels found between divergent platyrrhine genera, such as Aotus, Saimiriand Callimico.Using estimates of substitution rates of COII evolution in hominoid primates,the estimated date of divergence for the AotusCOII sequences is 3.6 million years. The AotusCOII data support the existence of multiple species of Aotus,with origins predating late Pleistocene climatic events. Although A. nancymaeand A. azaraeboth live south of the Amazon River and have been considered members of the same species group, phylogenetic analysis of the COII sequences does not support a close relationship between them.     

Systemic herpesvirus infection in an Azara's Night Monkey (Aotus azarae)

Background Intra‐ and inter‐species transmission of Human herpesvirus type 1 were noticed. In the present study, the herpesviral infection of a 1‐year‐old Azara’s Night Monkey (Aotus azarae) was investigated. Methods Immunohistochemistry and electron microscopy investigations were done. Results A fatal systemic herpesviral infection was demonstrated. Conclusion The results reveal the susceptibility of Azara’s Night Monkey to the Human herpesvirus type 1. Moreover, humans shedding herpes viral particles during the reactivation phase of the infection directly infect the Azara’s Night Monkeys.     

Chromosome localization and gene synteny of the major histocompatibility complex in the owl monkey,Aotus

Rodent cells were hybridized with owl monkey (Aotus) cells of karyotypes II, III, V, and VI. Aotus-rodent somatic hybrid lines preferentially segregating Aotus chromosomes were selected to determine the chromosomal location of the major histocompatibility complex and other genes with which it is syntenic in man. Based on correlation between concordant segregation of the chromosome as visualized by G-banding and expression of the Aotus antigens or enzymes in independent Aotus-rodent hybrid clones, we have assigned Aotus gene loci for the MHC, GLO, ME₁, SOD₂, and PGM₃ to Aotus chromosome 9 of karyotype VI (2n=49/50), chromosome 10 of karyotype V (2n=46), and chromosome 7 of karyotypes II and III (2n = 54 and 53). On the basis of banding patterns we previously postulated that these chromosomes of the different karyotypes were homologous. The gene assignments reported here provide independent evidence for that hypothesis. Aotus chromosomes 9 (K-VI), 10 (K-V), and 7 (K-II, III) are homologous to human chromosome 6 in that they all code for the MHC, GLO, ME₁, SOD₂, and PGM₃. The structural differences between these homologous chromosomes probably resulted from a pericentric inversion.Abbreviations used in this paper MHC major histocompatibility complex - HLA human lymphocyte antigen - PGM3 phosphoglucomutase-3 - ME₁ cytoplasmic malic enzyme-1 - SOD₂ superoxide dismutase-B - GLO glyoxalase 1 - OMLA owl monkey leukocyte antigens - K karyotype - ₂-M ₂-microglobulin - DMEM Dulbecco's modification of Eagle's medium - PEG polyethylene glycol - HAT hypoxanthine, aminopterin, and thymidine - KC1 potassium chloride - G-band-trypsin Giemsa band     

The normal and abnormal owl monkey (Aotus sp.) heart: looking at cardiomyopathy changes with echocardiography and electrocardiography

Background Cardiovascular disease, especially cardiomyopathy, was the major cause of death among owl monkeys (Aotus sp.) at a major colony and threatened colony sustainability. For this study, echocardiography (echo) and electrocardiography (ECG) normal values were established, and cardiomyopathy animals identified. Methods Forty‐eight owl monkeys were studied, 30 older than 10 years of age (‘aged’) and 8 of age 5 years (‘young’). Eight aged owl monkeys had cardiomyopathy. Results and Conclusions Aged Aotus had increased left ventricular posterior wall thickness over young animals. Left ventricular diameter and ejection fraction appeared to be the best identifying measurements for cardiomyopathy. There were no differences in the ECG.     

Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for human malaria parasites

 The New World primate Aotus nancymaae is susceptible to infection with the human malaria parasite Plasmodium falciparum and Plasmodium vivax and has therefore been recommended by the World Health Organization as a model for evaluation of malaria vaccine candidates. We present here a first step in the molecular characterization of the major histocompatibility complex (MHC) class II DRB genes of Aotus nancymaae (owl monkey or night monkey) by nucleotide sequence analysis of the polymorphic exon 2 segments. In a group of 15 nonrelated animals captivated in the wild, 34 MHC DRB alleles could be identified. Six allelic lineages were detected, two of them having human counterparts, while two other lineages have not been described in any other New World monkey species studied. As in the common marmoset, the diversity of DRB alleles appears to have arisen largely by point mutations in the β-pleated sheets and by frequent exchange of fixed sequence motifs in the α-helical portion. Pairs of alleles differing only at amino acid position b86 by an exchange of valine to glycine are present in Aotus, as in humans. Essential amino acid residues contributing to MHC DR peptide binding pockets number 1 and 4 are conserved or semiconserved between HLA-DR and Aona-DRB molecules, indicating a capacity to bind similar peptide repertoires. These results support fully our using Aotus monkeys as an animal model for evaluation of future subunit vaccine candidates. Received: 10 August 1999 / Revised: 11 October 1999     

Sequence and diversity of T-cell receptor alpha V, J, and C genes of the owl monkey Aotus nancymaae

 We cloned and sequenced TcR alpha chain cDNA of three healthy Aotus nancymaae monkeys. Fifteen different TRAJ segments and 9 different TRAV genes were identified in the 29 rearrangements analyzed. As expected from the greater phylogenetic distance, A. nancymaae TRA gene sequences diverged more from the human sequences than those of the chimpanzee or the rhesus macaque. However, no Aotus TRAJ segment or TRAV gene was found which lacked a human counterpart. These counterparts were AJ02, AJ05, AJ09, AJ15, AJ22, AJ23, AJ28, AJ30, AJ32, AJ34, AJ37, AJ40, AJ42, AJ45, AJ52 and AV2S1, AV2S3, AV3S1, AV8S1, AV12S1, AV15S1, ADV21S1/DV5, AV22S1S and AV23S1, respectively. In most cases the identity of amino acid sequences between corresponding Aotus and human genes was greater than 80%. This marked conservation of TRA gene sequences indicates a close structural relationship of Aotus and human TcR and demonstrates that the TcR repertoire in primates is remarkably stable. The results support the concept of using Aotus monkeys, which are susceptible to infection with the human malaria parasite Plasmodium falciparum, as an animal model for the evaluation of molecularly defined malaria vaccine candidates. Received: 15 January 1998 / Revised: 23 March 1998     

Genetic variability in natural populations of the Brazilian night monkey (Aotus infulatus)

Seventy-one night monkeys from both banks of the Tocantins River in Brazilian Amazonia were examined for 12 blood protein loci. The results indicate remarkable differences between the subpopulations of the two banks for the CA2, PGD, and GPI polymorphic systems. The average heterozygosity values of Aotusfor the west and east bank populations were 2.2 and 5.9, respectively. These results and the difficulties in delimiting species in this genus may indicate a relatively recent spur of evolutionary differentiation.     

Taxonomy of squirrel monkeys genus Saimiri (cebidae,platyrrhini): A preliminary report with description of a hitherto unnamed form

Two groups of squirrel monkeys, genus Saimiri, are distinguished by external characters. The first, or Roman type, contains Saimiri boliviensis of upper Amazonia south of the Rio Marañón-Amazonas, with two subspecies of which S. boliviensis peruviensis is described as new. The second group, or Gothic type, contains three species: Saimiri sciureus with four subspecies distributed over much of tropical South America, Saimiri ustus of Brazil between the south bank Amazonian Rios Purús and Xingu, and S. oerstedi isolated on a Pacific coastal area straddling Costa Rica and Panamá. The geographic range of S. sciureus overlaps parts of those of S. ustus and S. boliviensis. Incomplete karyotypic data indicate that the diploid number of chromosomes for the genus is 44. Geographic variation is characterized by reduction from seven to six or five paired acrocentric autosomes through pericentric inversion with reciprocal increase in number of paired submetacentric or subtelocentric autosomes. Geographic distribution, behavior, sexual dimorphism including dichromatism, and hybridization are discussed. Ventral guide hairs for orientation of subprecocial newborn toward the maternal mammae are described. Distinguishing characters of species and subspecies are provided in a key. The taxons are listed with the taxonomy of each discussed, their geographic distribution plotted and mapped.