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     

TheAotus from northern Argentina

Eight specimens ofAotus from Argentina were studied. Their geographic distribution, pelage phenotype, diploid number, chromosome measurements and morphology and C- and G-banding patterns have been reported in the present work. Cytogenetic analysis with Giemsa showed 2N=50 in the females and 2N=49 in a male. C- and G-banding patterns differed from those published for owl monkeys from other geographic regions.     

Reproduction of the owl monkey (Aotus spp.) in captivity

Abstract: The reproduction performance of captive owl monkeys, a breed used extensively in biomedical research, was observed at the Battelle Primate Facility (BPF). The colony grew through captive breeding, imports from the Peruvian Primatological Project, and others to a peak size of 730. It included seven karyotypes of Aotus sp. Results showed that owl monkeys can breed successfully in a laboratory in numbers sufficient to sustain modest research programs. Reproductive success increases when pairs are compatible, of the same karyotype, and stabilized; however, mated pairs of different karyotype are also productive. Under conditions of controlled lighting and heating, owl monkeys at BPF showed no birth peak nor birth season.     

Owl monkey MHC-DRB exon 2 reveals high similarity with several HLA-DRB lineages

One hundred and ten novel MHC-DRB gene exon 2 nucleotide sequences were sequenced in 96 monkeys from three owl monkey species (67 from Aotus nancymaae, 30 from Aotus nigriceps and 13 from Aotus vociferans). Owl monkeys, like humans, have high MHC-DRB allele polymorphism, revealing a striking similarity with several human allele lineages in the peptide binding region and presenting major convergence with DRB lineages from several Catarrhini (humans, apes and Old World monkeys) rather than with others New World monkeys (Platyrrhini). The parallelism between human and Aotus MHC-DRB reveals additional similarities regarding variability pattern, selection pressure and physicochemical constraints in amino acid replacements. These observations concerning previous findings of similarity between the Aotus immune system molecules and their human counterparts affirm this specie’s usefulness as an excellent animal model in biomedical research.Experiments carried out in this work complied with current Colombian Ministry of Health law and regulations governing animal care and handling.An erratum to this article can be found at     

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.     

Confirmed assignments of 15 structural gene loci to chromosomes of four owl monkey karyotypes

Fifteen gene loci for constitutive enzymes previously localized to specific owl monkey chromosomes of karyotypes III, V, and VI are confirmed by their assignments to homologous chromosomes of owl monkey karyotypes I, II, IV, and VII. The syntenic mapping of LDHA and GPI on a large metacentric, II-2, and the separate assignment of these two loci to two acrocentrics, I-9 and I-15, provide genetic evidence supporting the proposed fusion-fission event that characterized the karyotypic difference between owl monkeys inhabiting Colombia and the Panama Canal Zone. Moreover, the proposed hypothesis on chromosome polymorphism among the Colombian owl monkeys with karyotypes II, III, and IV, resulting from a fusion-fission event involving one metacentric and two subtelocentric pairs, is supported by the assignment of LDHB and MDH1 to the large metacentric I-2 and the separate localization of these two gene loci to II-13 and II-14, respectively.     

Behavior,Ecology, and Demography of <Emphasis Type="Italic">Aotus vociferans</Emphasis> in Yasuní National Park,Ecuador

Given its broad geographical distribution, Aotus is a productive genus for comparative studies that evaluate how different ecological factors influence the morphology, behavior, ecology, and demography of closely related species. During 18 mo we collected demographic, ranging, and activity data from owl monkeys (Aotus vociferans) in Yasuní National Park in eastern Ecuador. To collect demographic data, we monitored the trail system several times per week searching for groups. To characterize patterns of activity, we recorded the time when the subjects began and ended their nocturnal activity, and we collected data on range use and daily path length during 12 full-moon and 12 new-moon night follows of 1 radiocollared group. They ranged in size between 3 and 5 individuals (n = 4 groups). All groups were strictly nocturnal, beginning their activity between 1800 and 1900 h and finishing it between 0500 and 0600 h. The territory size of the radiocollared group was 6.3 ha. On average, the subjects traveled 645 m per night (±286 m) and ranged farther during full-moon than new-moon nights. The owl monkeys used a small number of preferred daytime sleeping trees. Our data conform well with previous studies of other tropical owl monkeys from Colombia and Perú. A comparison of tropical owl monkeys with more temperate Aotus azarai from the Argentinean Gran Chaco reveals that grouping patterns, day range length, and territory size are relatively conserved across the genus despite dramatic differences in body size and activity pattern.     

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).     

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.     

A putative homoeolog of human chromosome 12 in the owl monkey

Analyses of Southern blots of rodent x owl monkey somatic cell hybrids permitted syntenic assignment of gene loci coding for triosephosphate isomerase (TPI), antigen CD4(T4), Kirsten rat sarcoma 2(KRAS2) virus, insulin-like growth factor 1 (IGF1), and alpha 2-macroglobulin (A2M) to chromosome 10 of owl monkey karyotype VI(2n = 49, 50). In addition, regional in situ localization of the T4 and KRAS2 loci on the proximal region of the long arm of this acrocentric chromosome and on the corresponding homologous region on the long arm of metacentric chromosome 1 of karyotype IV (2n = 52) substantiated our hypothesis that a single fusion or fission event is responsible for the polymorphism in chromosome number characteristic of owl monkeys from at least three allopatric populations. The study supports a putative homoeology between owl monkey chromosome 10 (K-VI) and human chromosome 12. The morphological differences between these two primate chromosomes indicate evolutionary rearrangements involving at least one pericentric inversion.     

Karyotypic variation in susceptibility to hemolytic anemia and idiopathic eosinophilia of owl monkeys,Aotus trivirgatus

Hematologic data gathered over a period of 4.8 years from 196 owl monkeys,Aotus trivirgatus, were analyzed to find if karyotypic differences existed. It was found that none of 30 animals of karyotypes K-I and K-VI developed hemolytic anemia, whereas 46 of 99 animals of K-II, K-III and K-IV did (p<0.005). Analysis of hemograms of normal owl monkeys showed that mean percent eosinophils varied markedly, K-I monkeys having lowest counts, 3.2%, and K-VI animals having the highest, 33%. These results establish that idiopathic eosinophilia and hemolytic anemia in this species are probably unrelated but susceptibility to both has a strong genetic component.     

Moonstruck Primates: Owl Monkeys (Aotus) Need Moonlight for Nocturnal Activity in Their Natural Environment

Primates show activity patterns ranging from nocturnality to diurnality, with a few species showing activity both during day and night. Among anthropoids (monkeys, apes and humans), nocturnality is only present in the Central and South American owl monkey genus Aotus. Unlike other tropical Aotus species, the Azara''s owl monkeys (A. azarai) of the subtropics have switched their activity pattern from strict nocturnality to one that also includes regular diurnal activity. Harsher climate, food availability, and the lack of predators or diurnal competitors, have all been proposed as factors favoring evolutionary switches in primate activity patterns. However, the observational nature of most field studies has limited an understanding of the mechanisms responsible for this switch in activity patterns. The goal of our study was to evaluate the hypothesis that masking, namely the stimulatory and/or inhibitory/disinhibitory effects of environmental factors on synchronized circadian locomotor activity, is a key determinant of the unusual activity pattern of Azara''s owl monkeys. We use continuous long-term (6–18 months) 5-min-binned activity records obtained with actimeter collars fitted to wild owl monkeys (n = 10 individuals) to show that this different pattern results from strong masking of activity by the inhibiting and enhancing effects of ambient luminance and temperature. Conclusive evidence for the direct masking effect of light is provided by data showing that locomotor activity was almost completely inhibited when moonlight was shadowed during three lunar eclipses. Temperature also negatively masked locomotor activity, and this masking was manifested even under optimal light conditions. Our results highlight the importance of the masking of circadian rhythmicity as a determinant of nocturnality in wild owl monkeys and suggest that the stimulatory effects of dim light in nocturnal primates may have been selected as an adaptive response to moonlight. Furthermore, our data indicate that changes in sensitivity to specific environmental stimuli may have been an essential key for evolutionary switches between diurnal and nocturnal habits in primates.     

Multi-directional chromosome painting maps homologies between species belonging to three genera of New World monkeys and humans

We mapped chromosomal homologies in two species of Chiropotes (Pitheciini, Saki Monkeys) and one species of Aotus (Aotinae, Owl Monkey) by multi-directional chromosome painting. Human chromosome probes were hybridized to Chiropotes utahicki, C. israelita and Aotus nancymae metaphases. Wooly Monkey chromosome paints were also hybridized to Owl Monkey metaphases. We established Owl Monkey chromosome paint probes by flow sorting and reciprocally hybridized them to human chromosomes. The karyotypes of the Bearded Saki Monkeys studied here are close to the hypothesized ancestral platyrrhine karytoype, while that of the Owl Monkey appears to be highly derived. The A. nancymae karyotype is highly shuffled and only three human syntenic groups were found conserved coexisting with 17 derived human homologous associations. A minimum of 14 fissions and 13 fusions would be required to derive the A. nancymae karyotype from that of the ancestral New World primate karyotype. An inversion between homologs to segments of human 10 and 16 suggests a link between Callicebus and Chiropotes, while the syntenic association of 10/11 found in Aotus and Callicebus suggests a link between these two genera. Future molecular cytogenetic work will be needed to determine whether these rearrangements represent synapomorphic chromosomal traits.     

Reference strand conformational analysis (RSCA) is a valuable tool in identifying MHC-DRB sequences in three species of Aotus monkeys

The Aotus monkey has been of great value in the pre-clinical study of malaria vaccine candidates. Several components of this primate’s immune system have been studied and they display great similarity to their human counterparts. Cloning and sequencing studies have revealed extensive sequence polymorphisms in Aotus MHC-DRB with very high similarities to several human allelic lineages, grouping at least nine distinct MHC-DRB lineages. As the efficacy of peptide vaccines in this animal model may be strongly influenced by exon 2 MHC-DRB polymorphism, the availability of a reliable and rapid MHC-DRB typing method for three species of Aotus (Aotus nancymaae, Aotus vociferans and Aotus nigriceps) is necessary. Reference strand conformational analysis (RSCA) was used here for differentiating the distinctive Aotus MHC-DRB sequences’ mobility using five fluorescently labelled references proved to be very useful for resolving closely related sequences, establishing the number of sequences transcribed in a particular monkey and their identity. The RSCA method’s reliability in terms of identifying Aotus MHC-DRB sequences will facilitate evaluating individual responsiveness to vaccines and prompt studies associating susceptibility/resistance to infectious agents or auto-immune disease, for which Aotus monkeys may be considered to be an appropriate animal model.     

Chromosomes of thecercopithecus aethiops species group:C. aethiops (Linnaeus, 1758),C. cynosurus (Scopoli, 1786),C. pygerythrus (Cuvier, 1821), andC. sabaeus (Linnaeus, 1766)

The banded karyotypes of 34 monkeys of known geographic origin and belonging to the Cercopithecus aethiops group of species (C. aethiops, C. pygerythrus, C. cynosurus, C. sabaeus) show that chromosome evolution in this group is highly conservative. All species have 2n =60 chromosomes with very similar chromosome banding. However, differences were found both within and between species. A polymorphism of the NOR area of the “marked” chromosome pairs was found in all taxa (9 of 34 animals). All individuals referred to C. sabaeus,from both West Africa and the Barbados, are characterized by having highly positive G- and C- banded terminal sequences on chromosomes 7,10,12, and 14. Outgroup comparisons with other primates and a parsimony analysis suggest that these terminal bands are derived and are probably good taxonomic and phylogenetic indicators. Moreover, chromosome 18 is variable both between and within species in G banding and in short-arm length. The existence of within-species variation in karyotypes suggests that karyological comparisons must be based on adequate samples that include specimens coming from all the major geographic populations of the species concerned.     

A cytogenetic study on congenital limb malformations in the Japanese monkey (Macaca fuscata)

A cytogenetic investigation was performed on 88 Japanese monkeys (Macaca fuscata) with abnormal limbs from 11 free-ranging provisioned troops including nine individuals with abnormalities indistinguishable as to whether they were congenital or injurious. All of the monkeys with abnormal limbs including the nine questionable individuals had the same karyotypes as those of normal individuals. The chromosome number was 42, consisting of 20 bi-arm autosome pairs and a submetacentric X-chromosome and Y-chromosome. The ninth chromosome pair, which was the only chromosome pair with remarkable secondary constriction, displayed length polymorphism of the centromeric C-band and secondary constriction in both deformed and normal monkeys. These kinds of variants have also been commonly found in other monkey species, which have almost the same karyotype as the Japanese monkey and have not been reported to show frequent occurrence of limb malformation. We concluded therefore that chromosomal abnormalities could be excluded from the main causal factors for limb malformations of the Japanese monkey.     

Testing the weekend effect hypothesis: Time of day and lunar phase better predict the timing of births in laboratory‐housed primates than day of week

The weekend effect hypothesis proposes that captive primates are more likely to give birth during times of low disturbance and reduced staff activity. The hypothesis specifically predicts that laboratory‐housed primates will be more likely to give birth during the weekend than weekdays when staff activity is reduced. To date, support for the weekend effect hypothesis has been mixed and based on studies with relatively few subjects. To further examine the hypothesis, we analyzed the birthing patterns of three genera of laboratory‐housed primates: squirrel monkeys (Saimiri species, N = 2,090 births), owl monkeys (Aotus species, N = 479 births), and rhesus macaques (Macaca mulatta, N = 2,047 births). Contrary to predictions derived from the weekend effect hypothesis, the frequencies of births during weekends for all taxa were not significantly different from rates that would be expected by chance. However, while there was no variance across days of the week, all three taxa gave birth at nighttime, when staff was absent. This parallels reports of births in wild and captive monkeys, both diurnal and nocturnal, which are more likely to give birth during the night; plausibly a time when the environmental and social disturbance is lowest and the mother is safest to bond with her newborn infant. As all births occurred at night, we also explored the relationship between the lunar cycle and the timing of births timing. While the diurnal primates (i.e., Saimiri and Macaca) were no more likely to give birth on “bright” nights than “dark” nights, owl monkeys (Aotus) had a much higher frequency of births on bright nights than darker ones, and at rates that deviated from chance. Our data provide a more detailed understanding on how the environment may influence captive monkey births but do not support the oft‐cited weekend effect hypothesis.