The complete sequence and comparative analysis of ape sex chromosomes.

Apes possess two sex chromosomes-the male-specific Y chromosome and the X chromosome, which is present in both males and females. The Y chromosome is crucial for male reproduction, with deletions being linked to infertility1. The X chromosome is vital for reproduction and cognition2. Variation in mating patterns and brain function among apes suggests corresponding differences in their sex chromosomes. However, owing to their repetitive nature and incomplete reference assemblies, ape sex chromosomes have been challenging to study. Here, using the methodology developed for the telomere-to-telomere (T2T) human genome, we produced gapless assemblies of the X and Y chromosomes for five great apes (bonobo (Pan paniscus), chimpanzee (Pan troglodytes), western lowland gorilla (Gorilla gorilla gorilla), Bornean orangutan (Pongo pygmaeus) and Sumatran orangutan (Pongo abelii)) and a lesser ape (the siamang gibbon (Symphalangus syndactylus)), and untangled the intricacies of their evolution. Compared with the X chromosomes, the ape Y chromosomes vary greatly in size and have low alignability and high levels of structural rearrangements-owing to the accumulation of lineage-specific ampliconic regions, palindromes, transposable elements and satellites. Many Y chromosome genes expand in multi-copy families and some evolve under purifying selection. Thus, the Y chromosome exhibits dynamic evolution, whereas the X chromosome is more stable. Mapping short-read sequencing data to these assemblies revealed diversity and selection patterns on sex chromosomes of more than 100 individual great apes. These reference assemblies are expected to inform human evolution and conservation genetics of non-human apes, all of which are endangered species.

The structure, function and evolution of a complete human chromosome 8.

The complete assembly of each human chromosome is essential for understanding human biology and evolution1,2. Here we use complementary long-read sequencing technologies to complete the linear assembly of human chromosome 8. Our assembly resolves the sequence of five previously long-standing gaps, including a 2.08-Mb centromeric α-satellite array, a 644-kb copy number polymorphism in the ß-defensin gene cluster that is important for disease risk, and an 863-kb variable number tandem repeat at chromosome 8q21.2 that can function as a neocentromere. We show that the centromeric α-satellite array is generally methylated except for a 73-kb hypomethylated region of diverse higher-order α-satellites enriched with CENP-A nucleosomes, consistent with the location of the kinetochore. In addition, we confirm the overall organization and methylation pattern of the centromere in a diploid human genome. Using a dual long-read sequencing approach, we complete high-quality draft assemblies of the orthologous centromere from chromosome 8 in chimpanzee, orangutan and macaque to reconstruct its evolutionary history. Comparative and phylogenetic analyses show that the higher-order α-satellite structure evolved in the great ape ancestor with a layered symmetry, in which more ancient higher-order repeats locate peripherally to monomeric α-satellites. We estimate that the mutation rate of centromeric satellite DNA is accelerated by more than 2.2-fold compared to the unique portions of the genome, and this acceleration extends into the flanking sequence.

Phylogenetic differences in the morphology and shape of the central sulcus in great apes and humans: implications for the evolution of motor functions.

The central sulcus divides the primary motor and somatosensory cortices in many anthropoid primate brains. Differences exist in the surface area and depth of the central sulcus along the dorso-ventral plane in great apes and humans compared to other primate species. Within hominid species, there are variations in the depth and aspect of their hand motor area, or knob, within the precentral gyrus. In this study, we used post-image analyses on magnetic resonance images to characterize the central sulcus shape of humans, chimpanzees (Pan troglodytes), gorillas (Gorilla gorilla), and orangutans (Pongo pygmaeus and Pongo abelii). Using these data, we examined the morphological variability of central sulcus in hominids, focusing on the hand region, a significant change in human evolution. We show that the central sulcus shape differs between great ape species, but all show similar variations in the location of their hand knob. However, the prevalence of the knob location along the dorso-ventral plane and lateralization differs between species and the presence of a second ventral motor knob seems to be unique to humans. Humans and orangutans exhibit the most similar and complex central sulcus shapes. However, their similarities may reflect divergent evolutionary processes related to selection for different positional and habitual locomotor functions.

Relative leg-to-arm skeletal strength proportions in orangutans by species and sex.

Among extant great apes, orangutans climb most frequently. However, Bornean orangutans (Pongo pygmaeus) exhibit higher frequencies of terrestrial locomotion than do Sumatran orangutans (Pongo abelii). Variation in long bone cross-sectional geometry is known to reflect differential loading of the limbs. Thus, Bornean orangutans should show greater relative leg-to-arm strength than their Sumatran counterparts. Using skeletal specimens from museum collections, we measured two cross-sectional geometric measures of bone strength: the polar section modulus (Zpol) and the ratio of maximum to minimum area moments of inertia (Imax/Imin), at the midshaft of long bones in Bornean (n = 19) and Sumatran adult orangutans (n = 12) using medical CT and peripheral quantitative CT scans, and compared results to published data of other great apes. Relative leg-to-arm strength was quantified using ratios of femur and tibia over humerus, radius, and ulna, respectively. Differences between orangutan species and between sexes in median ratios were assessed using Wilcoxon rank sum tests. The tibia of Bornean orangutans was stronger relative to the humerus and the ulna than in Sumatran orangutans (p = 0.008 and 0.025, respectively), consistent with behavioral studies that indicate higher frequencies of terrestrial locomotion in the former. In three Zpol ratios, adult female orangutans showed greater leg-to-arm bone strength compared to flanged males, which may relate to females using their legs more during arboreal locomotion than in adult flanged males. A greater amount of habitat discontinuity on Borneo compared to Sumatra has been posited as a possible explanation for observed interspecific differences in locomotor behaviors, but recent camera trap studies has called this into question. Alternatively, greater frequencies of terrestriality in Pongo pygmaeus may be due to the absence of tigers on Borneo. The results of this study are consistent with the latter explanation given that habitat continuity was greater a century ago when our study sample was collected.

Evidence for the smallest fossil Pongo in southern China.

The rarity of Pongo fossils with precise absolute dating from the Middle Pleistocene hampers our understanding of the taxonomy and spatiotemporal distribution of Quaternary orangutans in southern China. Here, we report a newly discovered sample of 113 isolated teeth of fossil Pongo from Zhongshan Cave in the Bubing Basin, Guangxi, southern China. We describe the Pongo specimens from Zhongshan Cave and compare them metrically to other samples of fossil Pongo species (i.e., Pongo weidenreichi, Pongo devosi, Pongo duboisi, Pongo palaeosumatrensis, Pongo javensis, and Pongo sp.) and to extant orangutans (i.e., Pongo pygmaeus and Pongo abelii). The Zhongshan Pongo assemblage is dated using U-series and coupled electron spin resonance/U-series methods. Our results reasonably constrain the Zhongshan Pongo assemblage to 184 ± 16 ka, which is consistent with the biostratigraphic evidence. The Zhongshan Pongo teeth are only 6.5% larger on average than those of extant Pongo. The Zhongshan teeth are smaller overall than those of Pongo from all other cave sites in southern China, and they currently represent the smallest fossil orangutans in southern China. Based on their dental size, and the presence of a well-developed lingual pillar and lingual cingulum on the upper and lower incisors, an intermediate frequency of lingual cingulum remnants on the upper molars, and a higher frequency of moderate to heavy wrinkling on the upper and lower molars, we provisionally assign the Zhongshan fossils to P. devosi. Our results confirm earlier claims that P. weidenreichi is replaced by a smaller species in southern China, P. devosi, by the late Middle Pleistocene. The occurrence of P. devosi in Zhongshan Cave further extends its spatial and temporal distribution. The Pongo specimens from Zhongshan provide important new evidence to demonstrate that the dental morphological features of Pongo in southern China changed substantially during the late Middle Pleistocene.

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning.

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

MULTISPECIES SHIGELLA FLEXNERI OUTBREAK IN A ZOOLOGICAL COLLECTION COINCIDING WITH A CLUSTER IN THE LOCAL HUMAN POPULATION.

Shigella flexneri is a nonmotile gram-negative bacillus that affects humans and nonhuman primates. In August 2021, 15 primates at the ABQ BioPark demonstrated clinical signs of Shigella infection: 3 out of 4 Sumatran and hybrid orangutans (Pongo abelii), 6 out of 8 gorillas (Gorilla gorilla), 2 out of 9 chimpanzees (Pan troglodytes), and 4 out of 4 siamangs (Hylobates syndactylus). Three siamangs and one gorilla succumbed to complications of shigellosis during the initial outbreak and a chimpanzee died 10 mon later. Although it is well documented that Shigella may cause morbidity and mortality in nonhuman primates, the rapid and devastating nature of the outbreak, the difference from previous reports in zoological collections (enzootic vs outbreak), and the chronological overlap with the increase in human cases in the region makes discussion of this Shigella outbreak of significance. The cases presented here are significantly different than previous reports, because these were part of an outbreak that arose and subsided, versus other reports where the authors describe an enzootic disease with persistently infected animals. Close communication with the New Mexico Department of Health allowed for the investigation into possible sources of the outbreak, recommendations regarding biosecurity protocols, and staff education.

Biochemical and molecular confirmation of alkaptonuria in a Sumatran orangutan (Pongo abelii).

A 6-yr-old female orangutan presented with a history of dark urine that turned brown upon standing since birth. Repeated routine urinalysis and urine culture were unremarkable. Urine organic acid analysis showed elevation in homogentisic acid consistent with alkaptonuria. Sequence analysis identified a homozygous missense variant, c.1081G>A (p.Gly361Arg), of the homogentisate 1,2-dioxygenase (HGD) gene. Familial studies, molecular modeling, and comparison to human variant databases support this variant as the underlying cause of alkaptonuria in this orangutan. This is the first report of molecular confirmation of alkaptonuria in a nonhuman primate.

Middle Pleistocene Pongo from Ganxian Cave in southern China with implications for understanding dental size evolution in orangutans.

The Pongo fossil record of China extends from the Early Pleistocene to the Late Pleistocene, but to date, no late Middle Pleistocene samples of Pongo with precise absolute dating have been identified in southern China. Here, we report the recovery of 106 fossil teeth of Pongo from Ganxian Cave in the Bubing Basin, Guangxi, southern China. We dated the speleothems using Uranium-series and dated the two rhinoceros teeth using coupled electron spin resonance/Uranium-series dating methods to between 168.9 ± 2.4 ka and 362 ± 78 ka, respectively. These dates are consistent with the biostratigraphic and magnetostratigraphic age estimates. We further describe the fossil teeth from Ganxian Cave and compare them metrically to samples of fossil Pongo (i.e., Pongo weidenreichi, Pongo duboisi, Pongo palaeosumatrensis, Pongo javensis, and Pongo sp.) from the Early, Middle, and Late Pleistocene and to extant Pongo (i.e., Pongo pygmaeus and Pongo abelii) from Southeast Asia. Based on overall dental size, a high frequency of lingual cingulum remnants on the upper molars, and a low frequency of moderate to heavy wrinkling on the molars, we attribute the Ganxian fossils to P. weidenreichi. Compared with Pongo fossils from other mainland Southeast Asia sites, those from Ganxian confirm that dental size reduction of Pongo occurred principally during the Early and Middle Pleistocene. From the Middle to Late Pleistocene, all teeth except the P3 show little change in occlusal area, indicating that the size of these teeth remained relatively stable over time. The evolutionary trajectory of the Pongo dentition through time may be more complex than previously thought. More orangutan fossils with precise dating constraints are the keys to solving this issue.

Traces of dietary patterns in saliva of hominids: Profiling salivary amino acid fingerprints in great apes and humans.

Herbivorous animals that regularly consume tannin-rich food are known to secrete certain tannin-binding salivary proteins (TBSPs), especially proline-rich proteins and histidine-rich proteins, as an effective measure to counteract the antinutritive effects of dietary tannins. Due to their high binding capacity, TBSPs complex with tannins in the oral cavity, and thereby protect dietary proteins and digestive enzymes. Although the natural diet of great apes (Hominidae) is biased toward ripe fruits, analyses of food plants revealed that their natural diet contains considerable amounts of tannins, which is raising the question of possible counter-measures to cope with dietary tannins. In our study, we investigated the salivary amino acid profiles of zoo-housed Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii, and compared their results with corresponding data from Homo sapiens. Individual saliva samples of 42 apes and 17 humans were collected and quantitated by amino acid analysis, using cation-exchange chromatography with postcolumn derivatization, following acid hydrolysis. We found species-specific differences in the salivary amino acid profiles with average total salivary protein concentration ranging from 308.8 mg/dL in Po. abelii to 1165.6 mg/dL in G. gorilla. Total salivary protein was consistently higher in ape than in human saliva samples (174 mg/dL). All apes had on average also higher relative proline levels than humans did. Histidine levels had the highest concentration in the samples from Po. abelii followed by P. paniscus. In all ape species, the high salivary concentrations of proline and histidine are considered to be indicative of high concentrations of TBSPs in hominids. Given that the species differences in salivary composition obtained in this study correspond with overall patterns of secondary compound content in the diet of wild populations, we assume that salivary composition is resilient to acute and long-lasting changes in diet composition in general and tannin content in particular.

Single-inlet univentricular heart with persistent truncus arteriosus in a Sumatran orangutan (Pongo abelii).

Univentricular heart malformations are rarely described in the veterinary literature. This case report describes a single-inlet univentricular heart with persistent truncus arteriosus as a cause of death of a captive-bred, 2-day-old, female Sumatran orangutan (Pongo abelii), a critically endangered species.

Surgical placement of implantable cardiac loop recorders in great apes.

Cardiovascular disease is the leading cause of morbidity and mortality in zoologically managed adult great apes, accounting for 29%-77% of adult deaths in the North American population depending on the species. In an effort to better understand the underlying causes of heart disease, implantable loop recorders (ILRs) have been used in some cases to monitor great apes with suspected or known cases of arrhythmia. This is a 10-year review of the Great Ape Heart Project's experience of implanting 21 ILRs in 7 gorillas (Gorilla gorilla gorilla; 9 total ILR devices), 5 chimpanzees (Pan troglodytes, 11 total ILR devices), and 1 orangutan (Pongo abelii, 1 ILR device) in an effort to develop effective methods for surgical implantation and remote collection of the data for analysis.

Alternative reproductive tactics of unflanged and flanged male orangutans revisited.

In many slowly developing mammal species, males reach sexual maturity well before they develop secondary sexual characteristics. Sexually mature male orangutans have exceptionally long periods of developmental arrest. The two male morphs have been associated with behavioral alternative reproductive tactics, but this interpretation is based on cross-sectional analyses predominantly of Northwest Sumatran populations. Here we present the first longitudinal analyses of behavioral changes of 10 adult males that have been observed in both unflanged and flanged morph. We also analyzed long-term behavioral data on an additional 143 individually identified males from two study sites, Suaq (Sumatra, Pongo abelii) and Tuanan (Borneo, Pongo pygmaeus wurmbii), to assess male mating tactics cross-sectionally in relation to population, male morph (unflanged and flanged), and other socio-ecological factors. Both our longitudinal and cross-sectional results confirm and refine previous cross-sectional accounts of the differences in mating tactics between the unflanged and the flanged male morphs. In the unflanged morph, males exhibit higher sociability, particularly with females, and higher rates of both copulation and sexual coercion than in the flanged morph. Based on our results and those of previous studies showing that females prefer flanged males, and that flanged males have higher reproductive success, we conclude that unflanged males face a trade-off between avoiding male-male contest competition and gaining mating access to females, and thus follow a "best-of-a-bad-job" mating strategy.

MANAGEMENT OF ATRIAL FIBRILLATION, VENTRICULAR ARRHYTHMIA, LEFT VENTRICULAR DYSFUNCTION, AND SUBSEQUENT CARDIOPATHOLOGIC EVALUATION IN AN ORANGUTAN (PONGO PYGMAEUS × ABELII).

A 37-yr-old male vasectomized hybrid orangutan (Pongo pygmaeus × abelii) was diagnosed with left ventricular dysfunction during a preventative health care examination. Treatment was initiated with carvedilol. The following year, this orangutan was evaluated for intermittent lethargy. Following observation of an irregular cardiac rhythm during an echocardiogram, a lead II electrocardiogram revealed atrial fibrillation and ventricular arrhythmia. Additional treatment included amiodarone, furosemide, spironolactone, clopidogrel, and aspirin. An improved activity level was noted, and follow-up testing showed restoration of a sinus rhythm, reduced frequency of ventricular arrhythmia, and improved left ventricular function. The orangutan died 27 mon after initial diagnosis of heart disease, and a complete necropsy was performed. This article describes successful diagnosis and management of structural and arrhythmic heart disease in an orangutan, emphasizing the role of cardiac disease screening and behavioral training in apes, as well as the value of matching thorough antemortem and postmortem cardiac evaluation.

Naïve orangutans (Pongo abelii and Pongo pygmaeus) individually acquire nut-cracking using hammer tools.

Nut-cracking with hammer tools (henceforth: nut-cracking) has been argued to be one of the most complex tool-use behaviors observed in nonhuman animals. So far, only chimpanzees, capuchins, and macaques have been observed using tools to crack nuts in the wild (Boesch and Boesch, 1990; Gumert et al., 2009; Mannu and Ottoni, 2009). However, the learning mechanisms behind this behavior, and the extent of nut-cracking in other primate species are still unknown. The aim of this study was two-fold. First, we investigated whether another great ape species would develop nut-cracking when provided with all the tools and appropriate conditions to do so. Second, we examined the mechanisms behind the emergence of nut-cracking by testing a naïve sample. Orangutans (Pongo abelii and Pongo pygmaeus) have the second most extensive tool-use repertoire among the great apes (after chimpanzees) and show flexible problem-solving capacities. Orangutans have not been observed cracking nuts in the wild, however, perhaps because their arboreal habits provide limited opportunities for nut-cracking. Therefore, orangutans are a valid candidate species for the investigation of the development of this behavior. Four nut-cracking-naïve orangutans at Leipzig zoo (P. abelii; Mage = 16; age range = 10-19; 4F; at the time of testing) were provided with nuts and hammers but were not demonstrated the nut-cracking behavioral form. Additionally, we report data from a previously unpublished study by one of the authors (Martina Funk) with eight orangutans housed at Zürich zoo (six P. abelii and two P. pygmaeus; Mage = 14; age range = 2-30; 5F; at the time of testing) that followed a similar testing paradigm. Out of the twelve orangutans tested, at least four individuals, one from Leipzig (P. abelii) and three from Zürich (P. abelii and P. pygmaeus), spontaneously expressed nut-cracking using wooden hammers. These results demonstrate that nut-cracking can emerge in orangutans through individual learning and certain types of non-copying social learning.

Grouping behavior of Sumatran orangutans (Pongo abelii) and Tapanuli orangutans (Pongo tapanuliensis) living in forest with low fruit abundance.

In contrast to the African great apes, orangutans (Pongo spp.) are semisolitary: Individuals are often on their own, but form aggregations more often than expected by chance. These temporary aggregations provide social benefits such as mating opportunities. When fruit availability is high, costs of aggregating should be lower, because competition is less pronounced. Therefore, average party size is expected to be higher when fruit availability is high. This hypothesis would also explain why orangutans in highly fruit-productive habitats on Sumatra are more gregarious than in the usually less productive habitats of Borneo. Here, we describe the aggregation behavior of orangutans in less productive Sumatran habitats (Sikundur and Batang Toru), and compare results with those of previously surveyed field sites. Orangutans in Sikundur were more likely to form parties when fruit availability was higher, but the size of daily parties was not significantly affected by fruit availability. With regard to between-site comparisons, average party sizes of females and alone time of parous females in Sikundur and Batang Toru were substantially lower than those for two previously surveyed Sumatran sites, and both fall in the range of values for Bornean sites. Our results indicate that the assessment of orangutans on Sumatra as being more social than those on Borneo needs revision. Instead, between-site differences in sociality seem to reflect differences in average fruit availability.

Metacarpal trabecular bone varies with distinct hand-positions used in hominid locomotion.

Trabecular bone remodels during life in response to loading and thus should, at least in part, reflect potential variation in the magnitude, frequency and direction of joint loading across different hominid species. Here we analyse the trabecular structure across all non-pollical metacarpal distal heads (Mc2-5) in extant great apes, expanding on previous volume of interest and whole-epiphysis analyses that have largely focused on only the first or third metacarpal. Specifically, we employ both a univariate statistical mapping and a multivariate approach to test for both inter-ray and interspecific differences in relative trabecular bone volume fraction (RBV/TV) and degree of anisotropy (DA) in Mc2-5 subchondral trabecular bone. Results demonstrate that whereas DA values only separate Pongo from African apes (Pan troglodytes, Pan paniscus, Gorilla gorilla), RBV/TV distribution varies with the predicted loading of the metacarpophalangeal (McP) joints during locomotor behaviours in each species. Gorilla exhibits a relatively dorsal distribution of RBV/TV consistent with habitual hyper-extension of the McP joints during knuckle-walking, whereas Pongo has a palmar distribution consistent with flexed McP joints used to grasp arboreal substrates. Both Pan species possess a disto-dorsal distribution of RBV/TV, compatible with multiple hand postures associated with a more varied locomotor regime. Further inter-ray comparisons reveal RBV/TV patterns consistent with varied knuckle-walking postures in Pan species in contrast to higher RBV/TV values toward the midline of the hand in Mc2 and Mc5 of Gorilla, consistent with habitual palm-back knuckle-walking. These patterns of trabecular bone distribution and structure reflect different behavioural signals that could be useful for determining the behaviours of fossil hominins.

The loud scratch: a newly identified gesture of Sumatran orangutan mothers in the wild.

The communicative function of primates' self-directed behaviours like scratching has gained increasing attention in recent years, but their intentional use is still debated. Here, we addressed this issue by exploring the communicative function of 'loud scratches' in wild Sumatran orangutans. Building on previous studies in chimpanzees, we examined the prediction that audio-visual loud scratches are used communicatively in mother-infant travel coordination. Specifically, we examined whether individual, social and scratch features affected the use of pre-move scratches, markers of intentional signal use and approach responses. We analysed a total of 1457 scratching bouts, produced by 17 individuals (including four mothers and their dependent offspring) observed during 305 h of focal follows. Overall, we found that scratching bouts preceded departure mainly when these were produced by mothers and showed features of exaggeration. If the scratching individual was a mother, associates were more likely to be visually attentive during pre-move scratches than in other contexts. Approach or follow responses to scratches by individuals in association were predicted by context, the relationship with the scratcher (i.e. offspring) and the associate's attentional state. We conclude that orangutan mothers use loud scratches as communicative strategies to coordinate joint travel with their infants.

Perineal repair of a full-thickness rectal prolapse in a wild Sumatran orangutan (Pongo abelii).

A Delorme's procedure perineal surgical repair was performed in a wild adult male Sumatran orangutan (Pongo abelii) with a chronic persistent rectal prolapse that had been unsuccessfully treated by 6 previous surgeries. The rectal prolapse did not recur, and the orangutan was successfully released to the wild, 6 weeks later.