Colobine Species Research Articles

Reduction of bitter taste receptor gene family in folivorous colobine primates relative to omnivorous cercopithecine primates

Bitter taste perception is important in preventing animals from ingesting potentially toxic compounds. Whole-genome assembly (WGA) data have revealed that bitter taste receptor genes (TAS2Rs) comprise a multigene family with dozens of intact and disrupted genes in primates. However, publicly available WGA data are often incomplete, especially for multigene families. In this study, we employed a targeted capture (TC) approach specifically probing TAS2Rs for ten species of cercopithecid primates with diverse diets, including eight omnivorous cercopithecine species and two folivorous colobine species. We designed RNA probes for all TAS2Rs that we modeled to be intact in the common ancestor of cercopithecids (“ancestral-cercopithecid TAS2R gene set”). The TC was followed by short-read and high-depth massive-parallel sequencing. TC retrieved more intact TAS2R genes than found in WGA databases. We confirmed a large number of gene “births” at the common ancestor of cercopithecids and found that the colobine common ancestor and the cercopithecine common ancestor had contrasting trajectories: four gene “deaths” and three gene births, respectively. The number of intact TAS2R genes was markedly reduced in colobines (25–28 detected via TC and 20–26 detected via WGA analysis) as compared with cercopithecines (27–36 via TC and 19–30 via WGA). Birth or death events occurred at almost every phylogenetic-tree branch, making the composition of intact genes variable among species. These results show that evolutionary change in intact TAS2R genes is a complex process, refute a simple general prediction that herbivory favors more TAS2R genes, and have implications for understanding dietary adaptations and the evolution of detoxification abilities.

Black-and-white pelage as visually protective coloration in colobus monkeys

Conspicuous coloration is often seen as the evolutionary consequence of either sexual selection or warning predators visually about prey defences, although not all conspicuous species fit this paradigm. Exceptions include several species of colobus monkeys whose black-and-white coloration, characteristic of larger colobines, has never been explained. Here, using photographs of black-and-white colobus (Colobus vellerosus) taken in the wild, quantitative image analysis, and vision modelling (acuity-corrected feline, chimpanzee, and raptor vision), we provide evidence that their coloration provides distance-dependent camouflage in natural forest environments. At all viewing distances, black-and-white colobus monkeys blend into their environment because of their high chromatic overlap with the background when viewed by ecologically relevant predator vision models which have low visual acuities. Additionally, for chimpanzee and felid vision, there was evidence of edge disruption at longer viewing distances. Our comparative analyses of different species of colobines do not support an association between black-and-white coloration and larger body mass or group size, but this may simply be due to the limited number of species within the family. We reason that black-and-white colobines gain visually protective coloration through background matching against felids, and also benefit through disruptive coloration against felids and chimpanzees but rely on these protective coloration mechanisms less against raptors.Significance statementConspicuous black-and-white coloration in colobus monkeys has long eluded an evolutionary explanation. Our research, employing photographs of colobus monkeys, image analysis, and vision modelling, unveils a novel approach to this coloration. We show that in their natural forest habitats, black-and-white colobus monkeys employ distance-dependent camouflage against ecologically relevant predators with low visual acuity, blending in with the background at increasing viewing distances. In summary, the evolution of black-and-white colobus coloration appears to be related to background matching against felids, with added benefits of disruptive camouflage against felids and chimpanzees, less so to raptors, offering fresh insights into the complex interplay of coloration and survival strategies in mammals.

Leopard predation on wild Sichuan snub-nosed monkeys.

Predation is widely recognized as a powerful selective pressure on primate behavior and ecology, although knowledge of predator-prey relationships remains limited partly due to the rarity of directly observed attacks on primates. Here, we describe four confirmed or suspected instances of leopard (Panthera pardus) predation on free-ranging Sichuan (golden) snub-nosed monkeys (Rhinopithecus roxellana), a highly endangered colobine species endemic to China. We recorded predation events and the reactions of monkey group members. We suggest that the evolution of a multilevel society may be an adaptive response by Sichuan snub-nosed monkeys to the risk from leopards as well as other potential predators, one that balances the pressures of predation and intra-species competition and conflict.

Aspects of molar form and dietary proclivities of African colobines

This study investigates aspects of molar form in three African colobine species: Colobus polykomos, Colobus angolensis, and Piliocolobus badius. Our samples of C. polykomos and P. badius are from the Taï Forest, Ivory Coast; our sample of C. angolensis is from Diani, Kenya. To the extent that protective layers surrounding seeds are hard, we predicted that molar features related to hard-object feeding would be more pronounced in Colobus than they are Piliocolobus, as seed-eating generally occurs at higher frequencies in species of the former. We further predicted that among the colobines we studied, these features would be most pronounced in Taï Forest C. polykomos, which feeds on Pentaclethra macrophylla seeds encased within hard and tough seed pods. We compared overall enamel thickness, enamel thickness distribution, absolute crown strength, cusp tip geometry, and flare among molar samples. Sample sizes per species and molar type varied per comparison. We predicted differences in all variables except overall enamel thickness, which we expected would be invariant among colobines as a result of selection for thin enamel in these folivorous species. Of the variables we examined, only molar flare differed significantly between Colobus and Piliocolobus. Our findings suggest that molar flare, an ancient feature of cercopithecoid molars, was retained in Colobus but not in Piliocolobus, perhaps as a result of differences in the seed-eating proclivities of the two genera. Contrary to predictions, none of the aspects of molar form we investigated tracked current dietary differences in seed-eating between the two Colobus species. Finally, we explored the possibility that molar flare and absolute crown strength, when analyzed together, might afford greater differentiation among these colobine species. A multivariate t test of molar flare and absolute crown strength differentiated C. polykomos and P. badius, possibly reflecting known niche divergence between these two sympatric Taï Forest species.

Masticatory and ingestive effort in Procolobus verus, a small-bodied African colobine.

The olive colobus (Procolobus verus) is the smallest extant colobine. Based on the axiom that folivory is associated with larger body mass, the olive colobus is expected to be less folivorous than its sister taxon Piliocolobus badius, but previous studies show that the opposite is true. Here we test the hypothesis that masticatory and ingestive effort in the olive colobus is greater due to allometric factors related to bite force scaling and throughput of ingested foods. We analyzed oral processing data collected on olive colobus in the Taï Forest, Ivory Coast, between May 2016 and May 2018. We compare these with previously published data on P. badius and Colobus polykomos from Taï. In terms of overall feeding effort, olive colobus invest more effort (i.e., chewing cycles) than the larger colobines. When contrasts are restricted to commonly consumed foods, this greater energetic investment is not consistently observed. Ingestion of young leaves is associated with a reduced number of masticatory cycles in all three colobine species. A slightly elevated average effort in the olive colobus during young leaf feeding suggests this food source is more challenging in smaller monkeys, but mature leaf processing effort is generally the same among Taï colobines. Thus, for olive colobus, leaf ductility may be more problematic than leaf toughness in terms of masticatory effort. While there may be an allometric cost to being a small colobine, food selectivity is an important mitigating factor.

RETROSPECTIVE REVIEW OF UROLITHIASIS-RELATED MORBIDITY AND MORTALITY IN ASIAN COLOBINE MONKEYS.

Obstructive and incidental urolithiasis cases were evaluated in 5 Asian colobine monkey species (n= 21 individuals) that included 12 silvery langurs (Trachypithecus cristatus), 6 spectacled langurs (Trachypithecus obscurus), 1 Javan langur (Trachypithecus auratus auratus), 1 François' langur (Trachypithecus francoisi), and 1 red-shanked douc langur (Pygathrix nemaeus) from eight zoologic institutions. All institutions that responded were Association of Zoos and Aquariums, European Association of Zoos and Aquaria, or World Association of Zoos and Aquariums accredited. Males were more commonly represented in the total number of cases (86%), and all cases of obstructive urolithiasis occurred in males. The most common clinical signs observed in obstructive cases included stranguria (58.8%), lethargy (41.2%), anorexia (29.4%), depression (17.6%), and penile manipulation (11.8%). Clinicopathologic abnormalities revealed azotemia (76.5%), anemia (35.3%), and hyperkalemia (23.5%). Eleven of the 21 cases included urinalysis results, and crystalluria was reported in all 11. Obstructive cases were more commonly managed surgically, with medical management following. Instances of individual obstruction ranged from 0 (incidental finding) to 18, with a median of 8 (mean of 4.3) recurrent obstructions. A total of 39 urolith analyses were available from 17 of 21 cases, with calcium carbonate being the most common type isolated (37 of 39, 94.9%). Calcium oxalate was observed in the remaining 5.1% of cases (2 of 39). No cases exhibited a consistent match of crystalluria and urolith type. Death or euthanasia secondary to obstructive urolithiasis occurred in 52.4% of cases. Urinary obstruction secondary to urolithiasis appears to be a relevant cause of morbidity and mortality in Asian colobine species, and further study into etiology and preventive medicine should be undertaken.

Specialized digestive adaptations within the hindgut of a colobine monkey

In mammal herbivores, fiber digestion usually occurs predominantly in either the foregut or the hindgut. Reports of mechanisms showing synergistic function in both gut regions for the digestion of fiber and other nutrients in wild mammals are rare because it requires integrative study of anatomy, physiology, and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with high-fiber foods fermented primarily in their foreguts. A few colobine species live in temperate regions, so obtaining energy from fiber during the winter is essential. However, the mechanisms enabling this remain largely unknown. We hypothesized that such species possess specialized mechanisms to enhance fiber digestion in the hindgut and studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana. which is a temperate forest colobine from central China that experiences high-thermal-energy demands while restricted to a fibrous, low-energy winter diet. We tested for synergistic foregut and hindgut fiber digestion using comparisons of morphology, microbiome composition and function, and digestive efficiency. We found that the GSM colon has a significantly greater volume than that of other foregut-fermenting colobines. The microbiomes of the foregut and hindgut differed significantly in composition and abundance. However, while digestive efficiency and the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, both gut regions were dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. Our data suggest that both the GSM foregut and hindgut facilitate fiber digestion and that an enlarged colon is likely an adaptation to accommodate high throughput of fiber-rich food during winter.

Dental macrowear, diet, and anterior tooth use in Colobus polykomos and Piliocolobus badius

Two similarly-sized colobine species living sympatrically in the Ivory Coast's Taï Forest that differ in both diet and oral processing behavior provide an opportunity to explore the strength of associations between feeding behavior and dental wear patterns. Here we test the hypothesis that vigorous processing of tough, hard Pentaclethra macrophylla pods by Colobus polykomos manifests in greater anterior tooth wear relative to that observed in Piliocolobus badius, which does not exploit this resource. We assessed levels of anterior tooth wear in a sample of 160 upper incisors and 131 lower incisors from 18 adult Colobus polykomos and 62 adult Piliocolobus badius naturally deceased individuals from Taï National Park. We operationalized tooth wear by dividing the area of exposed dentin by total occlusal crown area. To assess relative degrees of incisor wear, we regressed incisor wear against molar wear (sample = 105 upper molars, 135 lower molars) for the pooled Colobus polykomos and Piliocolobus badius wear data and compared the number of individuals from each species that fell above and below the pooled regression curve for each model using Chi-square tests of independence and odds ratios. Under our hypothesis, we would expect more Colobus polykomos points above the pooled regression curve than Piliocolobus badius, indicating higher incisor wear relative to molar wear in Colobus polykomos. Nine of sixteen interspecific comparisons demonstrated this predicted pattern; however, none of the Chi-square tests or odds ratios were significant, indicating no difference between Colobus polykomos and Piliocolobusbadius incisor wear relative to molar wear. The absence of significant differences in incisor wear relative to molar wear highlights the challenge of identifying idiosyncratic feeding behavior in fossil taxa and the necessity for continued exploration of the relationship between diet and macrowear.

Apparent diet digestibility of captive colobines in relation to stomach types with special reference to fibre digestion

Colobine monkeys are known for the anatomical complexity of their stomachs, making them distinct within the primate order. Amongst foregut fermenters, they appear peculiar because of the occurrence of two different stomach types, having either three (‘tripartite’) or four (‘quadripartite’, adding the praesaccus) chambers. The functional differences between tri and quadripartite stomachs largely remain to be explained. In this study, we aim to compare the apparent digestibility (aD) in tripartite and quadripartite colobines. Hence, we measured the aD in two colobine species, Nasalis larvatus (quadripartite) and Trachypithecus cristatus (tripartite), in two zoos. We also included existing colobine literature data on the aD and analysed whether the aD of fibre components is different between the stomach types to test the hypothesis of whether quadripartite colobines show higher aD of fibre components than tripartite colobines did. Our captive N. larvatus specimen had a more distinctively varying nutrient intake across seasons with a larger seasonal variation in aD than that of a pair of T. cristatus, which mostly consumed commercial foods with a lower proportion of browse and less seasonal variation. We observed higher aD of dry matter (DM), neutral detergent fibre (NDF) and acid detergent fibre (ADF) in the N. larvatus specimen, suggesting a higher gut capacity of N. larvatus provided by the additional praesaccus forestomach chamber. Based on the analysis of literature data for aD, we also found that quadripartite species achieved higher fibre digestibility at similar dietary fibre levels compared with tripartite species, supporting the hypothesis that the additional gut capacity offered by the praesaccus facilitates a longer retention and hence more thorough microbial fermentation of plant fibre.

Multilevel societies facilitate infanticide avoidance through increased extrapair matings

In mammals characterized by a mating system in which a single male monopolizes reproduction, infanticide is reported to occur following a male take-over, often resulting in females returning to oestrus more rapidly than if their infant has survived. However, over the course of a 17-year study of golden snub-nosed monkeys, Rhinopithecus roxellana, a polygynous colobine species, we found no behavioural or suspected evidence of infanticide. Based on social network and genetic analyses, we found that more than half of the infants were sired as a result of extrapair matings (EPMs). Female golden snub-nosed monkeys initiated EPMs with bachelor or neighbouring resident males. These were considered ‘sneaky’ copulations because they did not occur in the presence of the leader male of the female's one-male unit (OMU). We suggest that through a process of paternity confusion, females decreased the likelihood of infanticide after a male take-over. In contrast, in a group of the same species in which the number of bachelor males was artificially reduced, EPMs were infrequent and four cases of infanticide were observed, three of them following a male take-over. Golden snub-nosed monkeys reside in a large multilevel society that develops by the fusion of several independent OMUs to form a breeding band, which is characterized by increased social cohesion and intrasexual tolerance among leader males. Females play an active role in mate choice, and engage in a diverse set of mating tactics, including counterstrategies such as EPMs to avoid infanticide. These results offer new insights into the diversity of behavioural strategies facilitated by complex social structures in nonhuman primates, as well as other social mammals.

Responses to Spatial and Temporal Variation in Food Availability on the Feeding Ecology of Proboscis Monkeys (Nasalis larvatus) in West Kalimantan, Indonesia

Folivorous primates have long been assumed to experience food competition less acutely than frugivores due to their ability to eat leaves, an abundant resource in most forest systems. Consequently, the behavioural responses of leaf-eating primates to variation in food availability are less well characterised than those of frugivores. Recent empirical studies have demonstrated that many colobine species are more affected by food availability and distribution than previously thought; they employ multiple strategies to survive during periods of food scarcity. We studied a population of proboscis monkeys (Nasalis larvatus) over 16 months in three forest types in West Kalimantan, Indonesia, to examine their responses to temporal fluctuation and spatial variation in food availability. We examined how feeding behaviour was influenced by the availability of plants in botanical plots to identify important and preferred foods of proboscis monkeys across months and in different forest types. Proboscis monkeys consumed foods from 68 genera, comprising 35% young leaves, 27% unripe fruit, 12% flowers and 6% mature leaves. Consumption of plant parts and genera by proboscis monkeys varied in response to monthly changes in food availability but did not vary among forest types despite substantial differences in phenology and floristics among them. The monkeys preferred unripe fruits and flowers and used young and mature leaves as fallback foods in mangrove forests. Documentation of proboscis monkey responses to variation in food availability contributes to our understanding of how monkeys respond to changes in their environments due to climate change and habitat degradation.

Cercopithecine and Colobine Abundance Across Protected and Unprotected Land in the Greater Mahale Ecosystem, Western Tanzania

Most primates live in unprotected land where abundances and threats may differ from those in protected areas. We therefore need to establish population densities in both unprotected and protected areas to effectively inform conservation planning. The Greater Mahale Ecosystem in western Tanzania is a region of mixed protected status with seven cercopithecine and colobine species: blue (Cercopithecus mitis doggetti), red-tailed (C. ascanius schmidi), and vervet (Chlorocebus pygerythrus) monkeys; ashy red colobus (Piliocolobus tephrosceles); black-and-white colobus (Colobus angolensis); and olive (Papio anubis) and yellow (P. cynocephalus) baboons. These species may be threatened by increasing human activity; however, except for ashy red colobus, no data on local abundances are available. We walked over 350 km of line transects in legally protected (Village Forest Reserves) and unprotected general land between August 2011 and October 2012 to estimate densities of primates and human activity. Primate densities were consistently low across the Greater Mahale Ecosystem. Blue and red-tailed monkey and ashy red colobus densities were especially low compared to populations in predominantly forested landscapes. Primate and human activity densities did not differ significantly inside and outside of reserves. Low primate densities could be natural responses to the lower proportions and quality of riparian forest habitat in the region. High levels of human activity and the absence of significantly higher primate densities in reserves suggest unprotected land could provide important refuges for primates in the Greater Mahale Ecosystem. This result further reinforces a broad need to include unprotected areas in primate conservation strategies.

A multi-level society comprised of one-male and multi-male core units in an African colobine (Colobus angolensis ruwenzorii).

Several mammalian species exhibit complex, nested social organizations, termed multi-level or modular societies. Multi-level societies comprise stable core units that fission and fuse with one another in a hierarchical manner, forming groups that vary in size over time. Among nonhuman primates, these social systems have been confirmed in several African papionin and Asian colobine species. We use data from August 2017 to July 2018 on individually-recognized Rwenzori Angolan colobus living near Lake Nabugabo, Uganda to document the first multi-level society in an African colobine. The study band comprised up to 135 individuals organized into 12 socially and spatially distinct core units that ranged in size from 4 to 23 individuals. These core units showed a strong affinity to one another, spending roughly 75% of their time together. Core units fissioned and fused non-randomly with one another throughout the day, leading to different combinations of core units being observed. Using association indices between core units, we employed hierarchical cluster analyses and permutation tests to show that some core units associated preferentially into clans. Thus, we confirm three tiers of social organization for Rwenzori Angolan colobus: core unit, clan, and band. The social organization of this subspecies is unlike any reported previously in a nonhuman primate, with about half the core units containing a single adult male and the others containing multiple reproductive adult males. The discovery of a unique primate multi-level society in a novel lineage could allow for a better understanding of the evolution of these complex social systems across the Animal Kingdom. Preliminary data show males transfer within the band and females transfer outside of the band, which is proposed for hominin multi-level societies. This subspecies could thus also provide insight into the selective pressures underlying multi-level societies in our own lineage.

A high-quality genome assembly for the endangered golden snub-nosed monkey (Rhinopithecus roxellana).

BackgroundThe golden snub-nosed monkey (Rhinopithecus roxellana) is an endangered colobine species endemic to China, which has several distinct traits including a unique social structure. Although a genome assembly for R. roxellana is available, it is incomplete and fragmented because it was constructed using short-read sequencing technology. Thus, important information such as genome structural variation and repeat sequences may be absent.FindingsTo obtain a high-quality chromosomal assembly for R. roxellana qinlingensis, we used 5 methods: Pacific Bioscience single-molecule real-time sequencing, Illumina paired-end sequencing, BioNano optical maps, 10X Genomics link-reads, and high-throughput chromosome conformation capture. The assembled genome was ∼3.04 Gb, with a contig N50 of 5.72 Mb and a scaffold N50 of 144.56 Mb. This represented a 100-fold improvement over the previously published genome. In the new genome, 22,497 protein-coding genes were predicted, of which 22,053 were functionally annotated. Gene family analysis showed that 993 and 2,745 gene families were expanded and contracted, respectively. The reconstructed phylogeny recovered a close relationship between R. rollexana and Macaca mulatta, and these 2 species diverged ∼13.4 million years ago.ConclusionWe constructed a high-quality genome assembly of the Qinling golden snub-nosed monkey; it had superior continuity and accuracy, which might be useful for future genetic studies in this species and as a new standard reference genome for colobine primates. In addition, the updated genome assembly might improve our understanding of this species and could assist conservation efforts.

The costs of competition: injury patterns in 2 Asian colobine monkeys

AbstractAggression rarely escalates to physical conflict because doing so puts individuals at risk of injury. Escalation only pays off when the potential benefits outweigh the potential costs, that is, when resources critical to fitness are at stake. Here, we investigated the occurrence of injury in 2 Asian colobine species: Nepal gray langurs (Semnopithecus schistaceus) and Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). In both species, younger individuals are higher-ranking and might have greater incentive to fight. However, Nepal gray langurs have a strict breeding season, which may magnify male mating competition, and Phayre’s leaf monkeys, unlike Nepal gray langurs, have female-biased dispersal, which may increase female injury risk during subadulthood. Using long-term data on observed injuries (Nepal gray langurs: n = 208; Phayre’s leaf monkeys: n = 225), we modeled the monthly occurrence of injury (Y/N) and found that males received more injuries than females in both species. Also, subadults generally experienced frequent injury, as young individuals likely face challenges when competing for group membership and/or establishing rank. In Nepal gray langurs, males received 3 times more injuries during the mating season, suggesting strong competition for mates during this period, and females experienced more injuries before conception, suggesting competition to meet the nutritional requirements for reproduction. Unexpectedly, females in smaller groups received more injuries in Nepal gray langurs. Overall, these results indicate that injuries are most likely when fighting may aid in establishing group membership, achieving high rank, and reproducing. Future research should investigate the influence of injuries on fitness outcomes.

Seed predation and passage time through the digestive tract of captive golden snub-nosed monkeys (Rhinopithecus roxellana)

Seed predation and dispersal by mammals are two key processes affecting the dynamics of plant populations and regeneration of forest trees. Colobine monkeys often consume fruits and are usually assumed to be seed predators, but their role as seed dispersers is unclear, especially dispersal universality of small seeds by colobine species. We conducted feeding experiments using the fruits of twelve tree species on four captive individuals of golden snub-nosed monkey (Rhinopithecus roxellana) at the breeding center in Shennongjia National Park. A large proportion of seeds (mean: 70.1%; range: 34.7–100.0%) were destroyed on passing through the digestive tract of the monkeys. The mean retention time (MRT) of seeds in the gut of monkeys was approximately 36 h (range: 28.4–41.7 h). Furthermore, the percentages of seed destruction (PSD) varied among plant species, as did the MRT. But neither PSD nor MRT was correlated with seed size. Golden snub-nosed monkeys appear to be both mild seed predators and potential seed dispersers, particularly of seeds less than 4.3 mm wide. The dispersal of seeds of Celastrus orbiculatus and Rubia ovatifolia may be positively affected by these primates. The role of colobine monkeys for seed dispersal need to be further attention in the future studies.

Nutrient intake and balancing among female Colobus angolensis palliatus inhabiting structurally distinct forest areas: Effects of group, season, and reproductive state.

Understanding intraspecific behavioral and dietary variation is critical for assessing primate populations' abilities to persist in habitats characterized by increasing anthropogenic disturbances. While it is evident that some species exhibit considerable dietary flexibility (in terms of species-specific plant parts) in relation to habitat disturbance, it is unclear if primates are characterized by similar variation and flexibility regarding nutrient intake. This study examined the effects of group, season, and reproductive state on nutrient intake and balancing in adult female Colobus angolensis palliatus in the Diani Forest, Kenya. During July 2014 to December 2015, estimates of nutrient intake were recorded for eight females from three groups inhabiting structurally and ecologically distinct forest areas differing in tree species composition and density. There were differences in metabolizable energy (ME) and macronutrient intakes among groups, seasons, and reproductive states. Most notably, females inhabiting one of the more disturbed forest areas consumed less ME and macronutrients compared to females in the more intact forest area. Contrary to prediction, females in early lactation consumed significantly less ME and macronutrients compared to non-lactating and late lactation females. Despite differences in macronutrient intake, the relative contribution of macronutrients to ME were generally more conservative among groups, seasons, and reproductive states. Average daily intake ratios of non-protein energy to available protein ranged from approximately 3.5:1-4.3:1 among groups. These results indicate that female C. a. palliatus demonstrate a consistent nutrient balancing strategy despite significant intergroup differences in consumption of species-specific plant parts. Data from additional colobine species inhabiting different forest types are required to assess the extent to which nutrient balancing is constrained by phylogeny or is more flexible to local ecological conditions.

Rapid emergence of independent \u201cchromosomal lineages\u201d in silvered-leaf monkey triggered by Y/autosome translocation

Sex/autosome translocations are rare events. The only known example in catarrhines is in the silvered-leaf monkey. Here the Y chromosome was reciprocally translocated with chromosome 1. The rearrangement produced an X1X2Y1Y2 sex chromosome system. At least three chromosomal variants of the intact chromosome 1 are known to exist. We characterized in high resolution the translocation products (Y1 and Y2) and the polymorphic forms of the intact chromosome 1 with a panel of more than 150 human BAC clones. We showed that the translocation products were extremely rearranged, in contrast to the high level of marker order conservation of the other silvered-leaf monkey chromosomes. Surprisingly, each translocation product appeared to form independent “chromosome lineages”; each having a myriad of distinct rearrangements. We reconstructed the evolutionary history of the translocation products by comparing the homologous chromosomes of two other colobine species: the African mantled guereza and the Indian langur. The results showed a massive reuse of breakpoints: only 12, out of the 40 breaks occurred in domains never reused in other rearrangements, while, strikingly, some domains were used up to four times. Such frequent breakpoint reuse if proved to be a general phenomenon has profound implications for mechanisms of chromosome evolution.

Fecal Nutrients Suggest Diets of Higher Fiber Levels in Free-Ranging than in Captive Proboscis Monkeys (Nasalis larvatus).

Understanding the natural diet of species may provide useful information that can contribute to successful captive maintenance. A common problem experienced with captive foregut-fermenting primate (colobine) diets is that they are deficient in fiber and therefore highly digestible. This may contribute to gastrointestinal disorders often observed in zoos. An approach to obtain information relevant for the improvement of diets is to compare the nutrient composition of feces from free-ranging and captive individuals. In theory, fecal material can be considered a proxy for diet intake integrated over a certain period of time. We collected fecal samples from eight free-ranging proboscis monkey (Nasalis larvatus, a highly endangered colobine species) groups from a secondary forest along the Kinabatangan River and four from a mixed mangrove-riverine forest along the Garama River, Sabah, Borneo, Malaysia. We also collected fecal samples from 12 individual captive adult/sub-adult proboscis monkeys from three different zoos. We confirmed that feces from free-ranging monkeys contained more fiber and less metabolic fecal nitrogen than those from captive specimens, indicating a less digestible diet in the wild. Modifying the diets of captive colobines to include more fiber, comparable to those of free-ranging ones, may contribute to their health and survival.

Evolution of Acidic Mammalian Chitinase Genes (CHIA) Is Related to Body Mass and Insectivory in Primates.

Insects are an important food resource for many primates, but the chitinous exoskeletons of arthropods have long been considered to be indigestible by the digestive enzymes of most mammals. However, recently mice and insectivorous bats were found to produce the enzyme acidic mammalian chitinase (AMCase) to digest insect exoskeletons. Here, we report on the gene CHIA and its paralogs, which encode AMCase, in a comparative sample of nonhuman primates. Our results show that early primates likely had three CHIA genes, suggesting that insects were an important component of the ancestral primate diet. With some exceptions, most extant primate species retain only one functional CHIA paralog. The exceptions include two colobine species, in which all CHIA genes have premature stop codons, and several New World monkey species that retain two functional genes. The most insectivorous species in our sample also have the largest number of functional CHIA genes. Tupaia chinensis and Otolemur garnettii retain three functional CHIA paralogs, whereas Tarsius syrichta has a total of five, two of which may be duplications specific to the tarsier lineage. Selection analyses indicate that CHIA genes are under more intense selection in species with higher insect consumption, as well as in smaller-bodied species (<500 g), providing molecular support for Kay's Threshold, a well-established component of primatological theory which proposes that only small primates can be primarily insectivorous. These findings suggest that primates, like mice and insectivorous bats, may use the enzyme AMCase to digest the chitin in insect exoskeletons, providing potentially significant nutritional benefits.