Chromosome Painting in Cercopithecus petaurista (Schreber, 1774) Compared to Other Monkeys of the Cercopithecini Tribe (Catarrhini, Primates).

The Cercopithecini tribe includes terrestrial and arboreal clades whose relationships are controversial, with a high level of chromosome rearrangements. In order to provide new insights on the tribe's phylogeny, chromosome painting, using the complete set of human syntenic probes, was performed in Cercopithecus petaurista, a representative species of the Cercopithecini tribe. The results show C. petaurista with a highly rearranged karyotype characterized by the fission of human chromosomes 1, 2, 3, 5, 6, 8, 11, and 12. These results compared with the literature data permit us to confirm the monophyly of the Cercopithecini tribe (fissions of chromosomes 5 and 6), as previously proposed by chromosomal and molecular data. Furthermore, we support the monophyly of the strictly arboreal Cercopithecus clade, previously proposed by the molecular approach, identifying chromosomal synapomorphies (fissions of chromosomes 1, 2, 3, 11, 12). We also add additional markers that can be useful for deciphering arboreal Cercopithecini phylogeny. For example, the fission of chromosome 8 is synapomorphy linking C. petaurista, C. erythrogaster, and C. nictitans among the arboreal species. Finally, a telomeric sequence probe was mapped on C. petaurista, showing only classic telomeric signals and giving no support to a previous hypothesis regarding a link between interspersed telomeric sequences in high rearranged genomes.

Oral Processing of Three Guenon Species in Taï National Park, Côte d'Ivoire.

Three guenon species in Taï National Park frequently form and maintain stable polyspecific associations despite significant feeding competition. This dietary overlap provides an opportunity to examine how closely related and anatomically similar taxa process the same foods. Our research examines whether the oral-processing behaviors of these guenons differ when they consume the same foods. Methods: Data on oral-processing behavior were collected on one habituated group each of Cercopithecus campbelli, C. diana, and C. petaurista in Taï National Park, Côte d'Ivoire from January 2016 to December 2018. We recorded the frequency with which foods were introduced to the mouth (ingestive action) and the frequency with which foods were processed using incisors, canines, and postcanine teeth. Oral-processing profiles for species-specific plant foods, fungi, and invertebrates were compared using Monte Carlo resampling. We quantified oral-processing behavior during a total of 2316 five-minute focal periods. Diana monkeys use their incisors significantly more per ingestive action than Campbell's monkeys or Lesser spot-nosed guenons. Lesser spot-nosed guenons use their incisors more than Campbell's monkeys. Diana monkeys also use significantly more post-canine chews per ingestive action than Campbell's monkeys and Lesser spot-nosed guenons. Lesser spot-nosed guenons generally use fewer post-canine chews than Diana monkeys but more than Campbell's monkeys. Canine use during feeding was rare in all three taxa. The three study species use different oral-processing profiles when consuming the same foods. These results are intriguing given the overall similarity in dental and cranial anatomy in these taxa. The oral-processing profiles we report do not encompass the full dietary breadth of all species; however, the behavioral diversity demonstrated during consumption of the same foods suggests that insight into feeding behavior is more likely obtained by examining oral processing of individual foods rather than broad food categories. Furthermore, these results underscore that important variation in feeding behavior is not necessarily associated with morphological differences in dental or craniofacial anatomy.

Simulated evolution of mating signal diversification in a primate radiation.

Divergence in allopatry and subsequent diversification of mating signals on secondary contact (reinforcement) is a major driver of phenotypic diversity. Observing this evolutionary process directly is often impossible, but simulated evolution can pinpoint key drivers of phenotypic variation. We developed evolutionary simulations in which mating signals, modelled as points in phenotype space, evolve across time under varying evolutionary scenarios. We model mate recognition signals in guenons, a primate radiation exhibiting colourful and diverse face patterns hypothesized to maintain reproductive isolation via mate choice. We simulate face pattern evolution across periods of allopatry and sympatry, identifying the role of key parameters in driving evolutionary endpoints. Results show that diversification in allopatry and assortative mate choice on secondary contact can induce rapid phenotypic diversification, resulting in distinctive (between species) and stereotyped (within species) face patterns, similar to extant guenons. Strong selection against hybrids is key to diversification, with even low levels of hybrid fitness often resulting in merged populations on secondary contact. Our results support a key role for reinforcement by assortative mating in the maintenance of species diversity and support the long-proposed prehistorical scenario for how such striking diversity was produced and maintained in perhaps the most colourful of all mammalian clades.

Occam's razor revisited: guenon species morphology supports evidence for an African influence in Bronze Age Aegean fresco primate iconography from Akrotiri, Thera.

In a recent exchange, Pareja et al. (Primates 61: 159-168, 2020a; Primates 61: 767-774, 2020b) and Urbani and Youlatos (Primates, https://doi.org/10.1007/s10329-020-00825-2 , 2020a) dispute the re-interpretation of the primate species depicted in a Bronze Age fresco from Room 6 of Building Complex Beta at Akrotiri, Thera. They review the history of interpretations of this artwork and combine the expertise of scholars that traditionally focus on such research with the scientific expertise of primatologists to reexamine the artwork. Additionally, they emphasize the morphological traits exhibited by these painted primates. We review and expand their list of candidate primates here in a decision table to demonstrate that the African link is better supported by the morphological traits than the Asian one proposed by Pareja et al. (2020a, b). Using such evidence, we show that other guenons of the tribe Cercopithecini, such as L'Hoest's monkey (Allochrocebus lhoesti) and the Diana monkey (Cercopithecus diana), provide equal support for the African link as the vervet monkey proposed by Urbani and Youlatos (2020a). However, the historical context supports the traditional interpretation that the Akrotiri fresco depicts vervet monkeys from this region. This discourse provides an open forum for scholars in various fields to contribute to an important problem that crosses disciplinary boundaries.

Population Genomics Reveals Incipient Speciation, Introgression, and Adaptation in the African Mona Monkey (Cercopithecus mona).

Guenons (tribe Cercopithecini) are the most widely distributed nonhuman primate in the tropical forest belt of Africa and show considerable phenotypic, taxonomic, and ecological diversity. However, genomic information for most species within this group is still lacking. Here, we present a high-quality de novo genome (total 2.90 Gb, contig N50 equal to 22.7 Mb) of the mona monkey (Cercopithecus mona), together with genome resequencing data of 13 individuals sampled across Nigeria. Our results showed differentiation between populations from East and West of the Niger River ∼84 ka and potential ancient introgression in the East population from other mona group species. The PTPRK, FRAS1, BNC2, and EDN3 genes related to pigmentation displayed signals of introgression in the East population. Genomic scans suggest that immunity genes such as AKT3 and IL13 (possibly involved in simian immunodeficiency virus defense), and G6PD, a gene involved in malaria resistance, are under positive natural selection. Our study gives insights into differentiation, natural selection, and introgression in guenons.

Oral Processing Behavior of Diana Monkeys (Cercopithecus diana) in Taï National Park, Côte d'Ivoire.

Primates are hypothesized to "fall back" on challenging-to-process foods when preferred foods are less available. Such dietary shifts may be accompanied by changes in oral processing behavior argued to be selectively important. Here, we examine the oral processing behavior of Diana monkeys (Cercopithecus diana) in the Taï Forest across their dietary breadth, testing relationships among food intake, fruit availability, preference, and oral processing behaviors including those involved in food ingestion and breakdown. We conducted 1,066 focal follows from April 2016 to September 2017 documenting frequencies of incisor, canine, and cheek tooth mastications (i.e., chews) per ingestive action (n = 11,906 feeding events). We used phenological survey and scan sample data collected between 2004 and 2009 to examine dietary preference and food availability. Our analyses show that Diana monkeys processed foods in significantly different ways (H2 = 360.8, p < 0.001), with invertebrates requiring the least oral processing, fruit requiring intermediate amounts, and leaves requiring the most oral processing. There was no relationship between fruit availability and consumption of preferred or nonpreferred fruits (p > 0.05); however, preferred fruits were processed with significantly fewer mastications (i.e., less chewing) than nonpreferred fruits (U = 6,557, p < 0.001). We thus demonstrate that, when preferred foods are scarce, Diana monkeys do not fall back on difficult-to-process foods. Changes in processing profiles occurred throughout the year and not solely when preferred foods were in short supply. Though preferred fruits required less processing than nonpreferred fruits, we found no relationship between fruit preference and fruit availability. Diana monkeys' lack of readily identifiable fallback foods may be attributable to the relatively high tree diversity and productivity of the Taï Forest. We conclude that Diana monkeys engage in resource switching, consuming a relatively easy-to-process diet year-round.

The structure of species discrimination signals across a primate radiation.

Discriminating conspecifics from heterospecifics can help avoid costly interactions between closely related sympatric species. The guenons, a recent primate radiation, exhibit high degrees of sympatry and form multi-species groups. Guenons have species-specific colorful face patterns hypothesized to function in species discrimination. Here, we use a machine learning approach to identify face regions most essential for species classification across fifteen guenon species. We validate these computational results using experiments with live guenons, showing that facial traits critical for accurate classification influence selective attention toward con- and heterospecific faces. Our results suggest variability among guenon species in reliance on single-trait-based versus holistic facial characteristics for species discrimination, with behavioral responses and computational results indicating variation from single-trait to whole-face patterns. Our study supports a role for guenon face patterns in species discrimination, and shows how complex signals can be informative about differences between species across a speciose and highly sympatric radiation.

The Genome of the Endangered Dryas Monkey Provides New Insights into the Evolutionary History of the Vervets.

Genomic data can be a powerful tool for inferring ecology, behavior, and conservation needs of highly elusive species, particularly, when other sources of information are hard to come by. Here, we focus on the Dryas monkey (Cercopithecus dryas), an endangered primate endemic to the Congo Basin with cryptic behavior and possibly <250 remaining adult individuals. Using whole-genome sequencing data, we show that the Dryas monkey represents a sister lineage to the vervets (Chlorocebus sp.) and has diverged from them ∼1.4 Ma with additional bidirectional gene flow ∼750,000-∼500,000 years ago that has likely involved the crossing of the Congo River. Together with evidence of gene flow across the Congo River in bonobos and okapis, our results suggest that the fluvial topology of the Congo River might have been more dynamic than previously recognized. Despite the presence of several homozygous loss-of-function mutations in genes associated with sperm mobility and immunity, we find high genetic diversity and low levels of inbreeding and genetic load in the studied Dryas monkey individual. This suggests that the current population carries sufficient genetic variability for long-term survival and might be larger than currently recognized. We thus provide an example of how genomic data can directly improve our understanding of highly elusive species.

Group-level competition influences urinary steroid hormones among wild red-tailed monkeys, indicating energetic costs.

Various theories emphasize that intergroup competition should affect intragroup cooperation and social relationships, especially if the cost of intergroup competition outweighs that of intragroup competition. This cost of intergroup competition may be quantified by changes in physiological status, such as in the steroid hormones cortisol (C) and testosterone (T), which rise or are depressed during periods of energetic stress, respectively. Here we tested for changes in urinary C and T after intergroup encounters (IGEs) among wild red-tailed monkeys (Cercopithecus ascanius), a species that experiences frequent intergroup feeding competition, at the Ngogo station in Kibale National Park, Uganda. We assayed 108 urine samples, of which 36 were collected after IGEs, from 23 individuals in four social groups. Bayesian multilevel models controlling for various confounds revealed that IGEs increased C and decreased T relative to baseline, consistent with an energetic cost to IGEs. The C change was more apparent in samples collected early after IGEs, suggesting an anticipatory increase, whereas the T change was stronger in later samples, suggesting sustained energetic trade-offs. Hormone responses were not affected by the IGE outcome. This cost to intergroup competition, together with little evidence for intragroup competition in redtails and other guenons, establishes an interesting test case for theories emphasizing the effect of intergroup competition on intragroup cooperation.

Dietary Variation in Diana Monkeys (Cercopithecus diana): The Effects of Polyspecific Associations.

Establishing dietary central tendencies and extremes remains an important goal of primate research. While habitat differences and spatial discontinuity are well-documented contributors to dietary variation, other factors including polyspecific associations may significantly impact diet through changes in strata use and/or increased feeding competition. Here, we examine polyspecific association with closely related species as a source of dietary variation in a rain forest primate. Diana monkeys (Cercopithecus diana) in Côte d'Ivoire's Taï Forest frequently participate in mixed-species groups. We use data collected over a 5-year period on 4 Diana monkey groups to examine how association affects group diets. Groups exhibited significant differences in association rates with other guenon species, but this minimally influenced diet when food categories (fruit, invertebrates, leaves) were compared: diet overlap of 4 groups across the study period ranges from 90.8 to 98.1%. Examination of species composition within food categories is more revealing: intergroup dietary overlap decreases to 69.8-79.4% across the study period when comparing species contributing to total frugivory and folivory. These data support earlier findings that Diana monkeys maintain fruit-rich diets by competitively excluding sympatric congeners while highlighting that even selective frugivores such as Diana monkeys may exhibit remarkable dietary flexibility. Our study underscores the fact that broad categorical labels can obscure significant dietary differences.

The evolution of the Cercopithecini: a (post)modern synthesis.

The Cercopithecini, or African guenon monkeys, are one of the most diverse clades of living primates and comprise the most species-rich clade of Catarrhini. Species identity is announced by flamboyant coloration of the facial and genital regions and, more cryptically, by vigorous chromosomal rearrangements among taxa. Beneath the skin, however, these animals are skeletally conservative and show low levels of genetic sequence divergence consonant with recent divergence between congeneric species. The guenons clearly demonstrate that morphological, cytogenetic, and reproductive differentiation proceed at different rates during speciation. We review diverse kinds of data in an effort to understand this conundrum.

Factors of influence and social correlates of parturition in captive Campbell's monkeys: Case study and breeding data.

How nonhuman primates deal with birth, at the moment of delivery, and during the following days, remains poorly explored because of the unpredictability of this event, particularly for forest-dwelling arboreal species. Available studies highlight intra- and interspecific variation which suggest flexibility of the timing of delivery, of behavior associated with labor contractions and parturition, and the social context and ambient noise surrounding delivery. Here, we present the findings of a two-decade survey of reproduction in a population of captive Campbell's monkeys. Analysis of 34 births (with a female-biased sex ratio) showed that deliveries occurred systematically at night and more frequently during week-ends and in fall (September-November). This suggests the existence of both circadian and infradian biological rhythms. We present the first detailed description of a birth for this species and its short-term social consequences. In line with previous findings for other monkeys and apes, labor (estimated by unusual stretching postures) and parturition were rapid, and delivery occurred in a clear social and vocal context. During the following days, the new mother became the center of attention of for young (kin and non-kin) females and rose through the hierarchy. We discuss socio-ecological factors, notably captivity conditions and the high degree of tolerance in the species' social system, and confirm the existence of both "rigidity" and "flexibility" in the primates' adaptive reproductive strategies.

The efficacy of sex-chromosomal markers in studies of Cercopithecus hybridization: Discovery of a captive hybrid and applications in wild populations.

We demonstrate the utility of previously described molecular methods for identifying hybrid Cercopithecus monkeys. Using phylogenetic analyses and DNA sequence comparisons at X-chromosomal and Y-chromosomal loci, we have identified a hybrid animal in the Cheyenne Mountain Zoo (USA)--an identification that was not known a priori but was later confirmed by review of zoo records. The molecular techniques employed here are of great use to studies of the genus Cercopithecus because, unlike most mammals, these monkeys frequently form polyspecific associations, and recent deforestation is likely to have driven otherwise low-level hybridization to higher frequencies which may reduce the fitness of threatened populations. Y-chromosomal markers are especially informative because they provide working hypotheses for (1) the primary mechanism of hybridization (i.e., species A males × species B females) and, by extension; (2) the major direction of gene flow.

Darting and marking techniques for an arboreal forest monkey, Cercopithecus ascanius.

Techniques are described for capturing and marking redtail monkeys (Cercopithecus ascanius). An air-powered darting rifle and syringe darts loaded with a Ketamine-Rompun mixture were used for capture. Ketamine was used for maintaining anesthesia. Monkeys were darted 48 times and captured 27 times. In 24 of the 27 captures, the monkeys were released unharmed. Adult males were marked with radiotransmitters attached to collars of nylon webbing. Females received nylon webbing collars with colorcoded plastic washers for identification.

Sexual dimorphism, mating system, and effect of phylogeny in De Brazza's monkey (Cercopithecus neglectus).

De Brazza's monkey (Cercopithecus neglectus), like other guenons, shows marked sexual dimorphism in an array of features. While strong sexual dimorphism is generally associated with a polygynous mating system, populations of De Brazza's monkeys in Gabon are reportedly monogamous. An explanation of this unique phenomenon is offered here. Patterns of sexual dimorphism are examined for morphology, growth and development, behavior, and ecology, and field and captive studies on the social organization and mating system of De Brazza's monkey and congeneric guenon species are reviewed. Based on the findings, it is postulated that 1) De Brazza's monkeys are not strictly monogamous, but exhibit interpopulational variation in their mating system, from facultative monogamy to mild polygyny; 2) marked sexual dimorphism most likely reflects the effect of the historical-phylogenetic factor; ie, it represents a holdover of a degree of dimorphism established earlier in evolutionary history when the degree of polygyny Was higher; and 3) lessening in the degree of polygyny and a tendency toward monogamy represents a consequence of selection toward small group size. Small group size, a unique antipredator strategy, and failure to form polyspecific associations are ultimately most likely the result of intragroup and interspecific competition and predation pressure.

Noninvasive measurement of blood pressure in African green monkeys (Cercopithecus aethiops).

Indirect measurements of arterial blood pressure were made in African green monkeys (Cercopithecus aethiops) employing a Doppler ultrasound stethoscope and standard cuff and an Infrasonde automatic blood pressure recorder. Measurements were obtained from anesthetized (10 mg/kg ketamine (HCI) and unanesthetized (1.5 mg/kg ketamine HCI) animals. Ketamine had no significant effect on blood pressure. Indirect measurements from the brachial artery were compared with direct femoral artery measurements and with each other. Systolic blood pressures measured by the Doppler (r = .948) and Infrasonde (r = .920) methods correlated closely with direct measurements but were significantly lower than systolic blood pressures measured by the direct method. Diastolic blood pressures measured by the Infrasonde method agreed closely with direct measurements (r = .947). Systolic blood pressures measured by the indirect methods correlated closely in both anesthetized (r = .973) and unanesthetized (r = .834) animals and were not significantly different. Mean blood pressures calculated from direct and Infrasonde measurements also correlated closely (r = .963), with direct measurements being 4 mmHg higher on the average. Mean blood pressures are less influenced by methodology and are more reproducible than other pressures. These noninvasive methods can be used to obtain simple and accurate measurements of blood pressure from anesthetized and unanesthetized monkeys and are of value in long-term studies in monkeys.