Animal behavior: A tale of two apes.

A new paper shows that rates of aggression are higher, and rates of coalition formation are lower, among male bonobos than among male chimpanzees. These findings are noteworthy because they challenge the view that female bonobos' preferences for less aggressive males favored a reduction in male aggression and an increase in social tolerance.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

Water scooping: tool use by a wild bonobo (Pan paniscus) at LuiKotale, a case report.

Tool use diversity is often considered to differentiate our two closest living relatives: the chimpanzee (Pan troglodytes) and the bonobo (P. paniscus). Chimpanzees appear to have the largest repertoire of tools amongst nonhuman primates, and in this species, many forms of tool use enhance food and water acquisition. In captivity, bonobos seem as adept as chimpanzees in tool use complexity, including in the foraging context. However, in the wild, bonobos have only been observed engaging in habitual tool use in the contexts of comfort, play, self-directed behaviour and communication, whilst no tool-assisted food acquisition has been reported. Whereas captive bonobos use tools for drinking, so far, the only report from the wild populations comes down to four observations of moss sponges used at Lomako. Here, we present the first report of tool use in the form of water scooping by a wild bonobo at LuiKotale. An adult female was observed and videotaped whilst using an emptied Cola chlamydantha pod to scoop and drink water from a stream. We discuss the conditions for such observations and the importance of looking out for rare behaviours and attempt to put the observation into the context of the opportunity versus necessity hypotheses. By adding novel information on tool use, our report contributes to the ongoing efforts to differentiate population-specific traits in the behavioural ecology of the bonobo.

Modulation of cell-mediated immunity during pregnancy in wild bonobos.

During pregnancy, the mammalian immune system must simultaneously protect against pathogens while being accommodating to the foreign fetal tissues. Our current understanding of this immune modulation derives predominantly from industrialized human populations and laboratory animals. However, their environments differ considerably from the pathogen-rich, resource-scarce environments in which pregnancy and the immune system co-evolved. For a better understanding of immune modulation during pregnancy in challenging environments, we measured urinary neopterin, a biomarker of cell-mediated immune responses, in 10 wild female bonobos (Pan paniscus) before, during and after pregnancy. Bonobos, sharing evolutionary roots and pregnancy characteristics with humans, serve as an ideal model for such investigation. Despite distinct environments, we hypothesized that cell-mediated immune modulation during pregnancy is similar between bonobos and humans. As predicted, neopterin levels were higher during than outside of pregnancy, and highest in the third trimester, with a significant decline post-partum. Our findings suggest shared mechanisms of cell-mediated immune modulation during pregnancy in bonobos and humans that are robust despite distinct environmental conditions. We propose that these patterns indicate shared immunological processes during pregnancy among hominins, and possibly other primates. This finding enhances our understanding of reproductive immunology.

Influence of food physical properties and environmental context on manipulative behaviors highlighted by new methodological approaches in zoo-housed bonobos (Pan paniscus).

Research on manipulative abilities in nonhuman primates, in the context of hominid evolution, has mostly focused on manual/pedal postures considered as static behaviors. While these behavioral repertoires highlighted the range of manipulative abilities in many species, manipulation is a dynamic process that mostly involves successive types of grips before reaching its goal. The present study aims to investigate the use of manual/pedal postures in zoo-housed bonobos in diverse dynamic food processing by using an innovative approach: the optimal matching analysis that compares sequences (i.e., succession of grasping postures) with each other. To characterize the manipulative techniques spontaneously employed by bonobos, we performed this sequential analysis of manual/pedal postures during 766 complete feeding sequences of 17 individuals. We analyzed the effectiveness with a score defined by a partial proxy of food intake (i.e., the number of mouthfuls) linked to a handling score measuring both the diversity and changes of manual postures during each sequence. We identified four techniques, used differently depending on the physical substrate on which the individual performed food manipulation and the food physical properties. Our results showed that manipulative techniques were more complex (i.e., higher handling score) for large foods and on substrates with lower stability. But the effectiveness score was not significantly lower for these items since manipulative complexity seemed to be compensated by a greater number of mouthfuls. It appeared that the techniques employed involved a trade-off between manipulative complexity and the amount of food ingested. This study allowed us to test and validate innovative analysis methods that are applicable to diverse ethological studies involving sequential events. Our results bring new data for a better understanding of the evolution of manual abilities in primates in association with different ecological contexts and both terrestrial and arboreal substrates and suggest that social and individual influences need to be explored further.

Future coexistence with great apes will require major changes to policy and practice.

The great apes-bonobos, chimpanzees, gorillas and orangutans-are critically threatened by human activities. We have destroyed their habitats, hunted them and transmitted fatal diseases to them. Yet we also conduct research on them, try to protect them and live alongside them. They are endangered, and time is running out. Here we outline what must be done to ensure that future generations continue to share this planet with great apes. We urge dialogue with those who live with great apes and interact with them often. We advocate conservation plans that acknowledge the realities of climate change, economic drivers and population growth. We encourage researchers to use technology to minimize risks to great apes. Our proposals will require substantial investment, and we identify ways to generate these funds. We conclude with a discussion of how field researchers might alter their work to protect our closest living relatives more effectively.

Stubby versus stabby: A preliminary analysis of canine microwear in primates: Implication for inferring ingestive behaviors.

Molar and incisor microwear reflect aspects of food choice and ingestive behaviors in living primates and have both been used to infer the same for fossil samples. Canine microwear, however, has received less attention, perhaps because of the prominent role canines play in social display and because they are used as weapons-while outside of a few specialized cases, their involvement in diet related behaviors has not been obvious. Here, we posit that microwear can also provide glimpses into canine tooth use in ingestion. Canines of Sumatran long-tailed macaques (Macaca fascicularis), agile gibbons (Hylobates agilis), lar gibbons (Hylobates lar), Thomas' leaf monkeys (Presbytis thomasi), and orangutans (Pongo abelii), and two African great apes, bonobos (Pan paniscus) and common chimpanzees (Pan troglodytes schweinfurthii), were considered. The labial tips of maxillary canine replicas were scanned using a white-light confocal profiler, and both feature and texture analyses were used to characterize microwear surface patterning. The taxa exhibited significant differences in canine microwear. In some cases, these were consistent with variation in reported anterior tooth use such that, for example, the orangutans, known to use their front teeth extensively in ingestion, had the highest median number of microwear features on their canines, whereas the gibbons, reported to use their front teeth infrequently in food acquisition, had the lowest.

Apes able to recognise faces after quarter of a century.

Recent research has provided evidence for the longest-lasting non-human social memory ever documented - in bonobos and chimpanzees. Arabella Gray finds out more about the study.

Vertical climbing in free-ranging bonobos: An exploratory study integrating locomotor performance and substrate compliance.

OBJECTIVES: Ecological factors and body size shape animal movement and adaptation. Large primates such as bonobos excel in navigating the demanding substrates of arboreal habitats. However, current approaches lack comprehensive assessment of climbing performance in free-ranging individuals, limiting our understanding of locomotor adaptations. This study aims to explore climbing performance in free-ranging bonobos and how substrate properties affect their behavior. METHODS: We collected data on the climbing performance of habituated bonobos, Pan paniscus, in the Bolobo Territory, Democratic Republic of Congo. We analyzed 46 climbing bouts (12 ascents, 34 descents) while moving on vertical substrates of varying diameter and compliance levels. This study assessed the average speed, peak acceleration, resting postures, and transitions between climbing and other locomotor modes. RESULTS: During climbing sequences and transitions, bonobos mitigate speed variations. They also exhibit regular pauses during climbing and show higher speeds during descent in contrast to their ascent. Regarding the influence of substrate properties, bonobos exhibit higher speed when ascending on thin and slightly flexible substrates, while they appear to achieve higher speeds when descending on large and stiff substrates, by using a "fire-pole slide" submode. DISCUSSION: Bonobos demonstrate remarkable abilities for negotiating vertical substrates and substrate properties influence their performance. Our results support the idea that bonobos adopt a behavioral strategy that aligns with the notion of minimizing costs. Overall, the adoption of high velocities and the use of low-cost resting postures may reduce muscle fatigue. These aspects could represent important targets of selection to ensure ecological efficiency in bonobos.

Rethinking peace from a bonobo perspective.

Reconstructing pathways to human peace can be hampered by superficial evaluations of similar processes in nonhuman species. A deeper understanding of bonobo social systems allows us to reevaluate the preconditions for peace to gain a greater insight on the evolutionary timescale of peace emergence.

Functional host-specific adaptation of the intestinal microbiome in hominids.

Fine-scale knowledge of the changes in composition and function of the human gut microbiome compared that of our closest relatives is critical for understanding the evolutionary processes underlying its developmental trajectory. To infer taxonomic and functional changes in the gut microbiome across hominids at different timescales, we perform high-resolution metagenomic-based analyzes of the fecal microbiome from over two hundred samples including diverse human populations, as well as wild-living chimpanzees, bonobos, and gorillas. We find human-associated taxa depleted within non-human apes and patterns of host-specific gut microbiota, suggesting the widespread acquisition of novel microbial clades along the evolutionary divergence of hosts. In contrast, we reveal multiple lines of evidence for a pervasive loss of diversity in human populations in correlation with a high Human Development Index, including evolutionarily conserved clades. Similarly, patterns of co-phylogeny between microbes and hosts are found to be disrupted in humans. Together with identifying individual microbial taxa and functional adaptations that correlate to host phylogeny, these findings offer insights into specific candidates playing a role in the diverging trajectories of the gut microbiome of hominids. We find that repeated horizontal gene transfer and gene loss, as well as the adaptation to transient microaerobic conditions appear to have played a role in the evolution of the human gut microbiome.

Understanding others' preferences: A comparison across primate species and human societies.

We investigated children's and non-human great apes' ability to anticipate others' choices from their evident food preferences-regardless of whether these preferences deviate or align with one's own. We assessed children from three culturally-diverse societies (Namibia, Germany, and Samoa; N = 71; age range = 5-11) and four non-human great ape species (chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii); N = 25; age range = 7-29) regarding their choices in a dyadic food-retrieval task. Across conditions, participants' preferences were either aligned (same preference condition) or opposed (opposite preference condition) to those of their competitors. Children across societies altered their choices based on their competitor's preferences, indicating a cross-culturally recurrent capacity to anticipate others' choices relying on preferences-based inferences. In contrast to human children, all non-human great apes chose according to their own preferences but independent of those of their competitors. In sum, these results suggest that the tendency to anticipate others' choices based on their food preferences is cross-culturally robust and, among the great apes, most likely specific to humans.

The deep trabecular structure of first metacarpals in extant hominids.

OBJECTIVES: Recent studies have associated subarticular trabecular bone distribution in the extant hominid first metacarpal (Mc1) with observed thumb use, to infer fossil hominin thumb use. Here, we analyze the entire Mc1 to test for interspecific differences in: (1) the absolute volume of trabecular volume fraction, (2) the distribution of the deeper trabecular network, and (3) the distribution of trabeculae in the medullary cavity, especially beneath the Mc1 disto-radial flange. MATERIALS AND METHODS: Trabecular bone was imaged using micro-computed tomography in a sample of Homo sapiens (n = 11), Pan paniscus (n = 10), Pan troglodytes (n = 11), Gorilla gorilla (n = 10) and Pongo sp., (n = 7). Using Canonical Holistic Morphometric Analysis (cHMA), we tested for interspecific differences in the trabecular bone volume fraction (BV/TV) and its relative distribution (rBV/TV) throughout the Mc1, including within the head, medullary cavity, and base. RESULTS: P. paniscus had the highest, and H. sapiens the lowest, BV/TV relative to other species. rBV/TV distribution statistically distinguished the radial concentrations and lack of medullary trabecular bone in the H. sapiens Mc1 from all other hominids. H. sapiens and, to a lesser extent, G. gorilla also had a significantly higher trabecular volume beneath the disto-radial flange relative to other hominids. DISCUSSION: These results are consistent with differences in observed thumb use in these species and may also reflect systemic differences in bone volume fraction. The trabecular bone extension into the medullary cavity and concentrations beneath the disto-radial flange may represent crucial biomechanical signals that will aid in the inference of fossil hominin thumb use.

Captive bonobos (Pan paniscus) apply precision grips when using flaked stone tools.

OBJECTIVES: Current evidence suggests that flaked stone tool technologies did not emerge until ~3.3-2.6 million-years-ago (Ma). It is often hypothesized that early hominin (principally Ardipithecus and early Australopithecus) manual anatomy may have prevented an earlier emergence, as the forceful precision grips essential to flake tool-use may have been ineffectively performed by these species. Marzke, Marchant, McGrew, and Reece (2015) observed potentially forceful pad-to-side precision grips being recruited by wild chimpanzees (Pan troglodytes) during feeding behaviors, indicating that Pan-like manual anatomy, and therefore potentially early hominin anatomy, may be capable of effectively securing flake stone tools during their use. MATERIALS AND METHODS: Here, we report on the grips recruited by four captive, human-trained, bonobos (Pan paniscus) during the use of stone and organic tools, including flake stone tools during cutting behaviors. RESULTS: It is revealed that pad-to-side precision grips are frequently recruited by these bonobos when securing stone flakes during cutting actions. In some instances, high forces could have been resisted and applied by the thumb and fingers. DISCUSSION: While our analyzes are preliminary and limited to captive individuals, and Pan is not suggested to secure flakes with the same efficacy as Homo or Australopithecus, it points to early hominins potentially being able to perform the precision grips required to use flake stone tools. In turn, the ability to gain tangible benefits from the effective use of flake tools (i.e., gain energetic returns from processing food resources) may have been - at least anatomically - possible in early Australopithecus and other pre-Early Stone Age hominin species. In turn, hominin manual anatomy may not be a leading restriction on the emergence of the earliest stone tool technologies.

Morphological integration and shape covariation between the trapezium and first metacarpal among extant hominids.

OBJECTIVES: The shape of the trapezium and first metacarpal (Mc1) markedly influence thumb mobility, strength, and the manual abilities of extant hominids. Previous research has typically focused solely on trapezium-Mc1 joint shape. Here we investigate how morphological integration and shape covariation between the entire trapezium (articular and non-articular surfaces) and the entire Mc1 reflect known differences in thumb use in extant hominids. MATERIALS AND METHODS: We analyzed shape covariation in associated trapezia and Mc1s across a large, diverse sample of Homo sapiens (n = 40 individuals) and other extant hominids (Pan troglodytes, n = 16; Pan paniscus, n = 13; Gorilla gorilla gorilla, n = 27; Gorilla beringei, n = 6; Pongo pygmaeus, n = 14; Pongo abelii, n = 9) using a 3D geometric morphometric approach. We tested for interspecific significant differences in degree of morphological integration and patterns of shape covariation between the entire trapezium and Mc1, as well as within the trapezium-Mc1 joint specifically. RESULTS: Significant morphological integration was only found in the trapezium-Mc1 joint of H. sapiens and G. g. gorilla. Each genus showed a specific pattern of shape covariation between the entire trapezium and Mc1 that was consistent with different intercarpal and carpometacarpal joint postures. DISCUSSION: Our results are consistent with known differences in habitual thumb use, including a more abducted thumb during forceful precision grips in H. sapiens and a more adducted thumb in other hominids used for diverse grips. These results will help to infer thumb use in fossil hominins.

OpenApePose, a database of annotated ape photographs for pose estimation.

Because of their close relationship with humans, non-human apes (chimpanzees, bonobos, gorillas, orangutans, and gibbons, including siamangs) are of great scientific interest. The goal of understanding their complex behavior would be greatly advanced by the ability to perform video-based pose tracking. Tracking, however, requires high-quality annotated datasets of ape photographs. Here we present OpenApePose, a new public dataset of 71,868 photographs, annotated with 16 body landmarks of six ape species in naturalistic contexts. We show that a standard deep net (HRNet-W48) trained on ape photos can reliably track out-of-sample ape photos better than networks trained on monkeys (specifically, the OpenMonkeyPose dataset) and on humans (COCO) can. This trained network can track apes almost as well as the other networks can track their respective taxa, and models trained without one of the six ape species can track the held-out species better than the monkey and human models can. Ultimately, the results of our analyses highlight the importance of large, specialized databases for animal tracking systems and confirm the utility of our new ape database.

All animals carry out a wide range of behaviors in everyday life, such as feeding and communicating with one another. Understanding the complex behavior of non-human apes such as chimpanzees, bonobos, gorillas, orangutans, and various gibbons is of great interest to scientists due to their close relationship with humans. Each behavior is made up of a string of poses that an animal makes with its body. To analyze them in a reliable and consistent way, scientists have developed automated pose estimation methods that determine the position of body parts from photographs and videos. While these systems require minimal external input to perform, they need to be trained on a large dataset of high-quality annotated images of the target animals to teach the system what to look for. So far, scientists have relied on systems trained on monkey and human images to analyze ape data. However, apes are particularly challenging to track because their body textures are uniform, and they have a large number of poses. Therefore, for the most accurate tracking of ape behaviors, a dedicated training dataset of annotated ape images is required. Desai et al. filled this gap by creating the "OpenApePose" dataset, which contains 71,868 photographs of apes from six species, annotated using 16 body landmarks. To test the dataset, the researchers trained an artificial intelligence network on separate monkey, human and ape datasets. The findings showed that the network is better at tracking apes when trained on ape images rather than those of monkeys or humans. It is also equally good at tracking apes as other monkey and human networks are at tracking their own species. This is contrary to optimistic expectations that monkey and human models could be generalized to apes. Training the network without images of one of the six ape species showed that it can still track the excluded species better than monkey and human models can. These experiments highlight the importance of species and family-specific datasets. OpenApePose is a valuable resource for researchers from various fields. It can aid tracking of animal behavior in the wild using large quantities of footage recorded by camera traps and drones. Artificial intelligence models trained on the OpenApePose dataset could also help scientists ­ such as neuroscientists ­ link movement with other types of data, including brain activity measurements, to gain deeper insights into behavior.

Bonobos and chimpanzees remember familiar conspecifics for decades.

Recognition and memory of familiar conspecifics provides the foundation for complex sociality and is vital to navigating an unpredictable social world [Tibbetts and Dale, Trends Ecol. Evol. 22, 529-537 (2007)]. Human social memory incorporates content about interactions and relationships and can last for decades [Sherry and Schacter, Psychol. Rev. 94, 439-454 (1987)]. Long-term social memory likely played a key role throughout human evolution, as our ancestors increasingly built relationships that operated across distant space and time [Malone et al., Int. J. Primatol. 33, 1251-1277 (2012)]. Although individual recognition is widespread among animals and sometimes lasts for years, little is known about social memory in nonhuman apes and the shared evolutionary foundations of human social memory. In a preferential-looking eye-tracking task, we presented chimpanzees and bonobos (N = 26) with side-by-side images of a previous groupmate and a conspecific stranger of the same sex. Apes' attention was biased toward former groupmates, indicating long-term memory for past social partners. The strength of biases toward former groupmates was not impacted by the duration apart, and our results suggest that recognition may persist for at least 26 y beyond separation. We also found significant but weak evidence that, like humans, apes may remember the quality or content of these past relationships: apes' looking biases were stronger for individuals with whom they had more positive histories of social interaction. Long-lasting social memory likely provided key foundations for the evolution of human culture and sociality as they extended across time, space, and group boundaries.

Auditory thresholds compatible with optimal speech reception likely evolved before the human-chimpanzee split.

The anatomy of the auditory region of fossil hominins may shed light on the emergence of human spoken language. Humans differ from other great apes in several features of the external, middle and inner ear (e.g., short external ear canal, small tympanic membrane, large oval window). However, the functional implications of these differences remain poorly understood as comparative audiometric data from great apes are scarce and conflicting. Here, we measure the sound transfer function of the external and middle ears of humans, chimpanzees and bonobos, using laser-Doppler vibrometry and finite element analysis. This sound transfer function affects auditory thresholds, which relate to speech reception thresholds in humans. Unexpectedly we find that external and middle ears of chimpanzees and bonobos transfer sound better than human ones in the frequency range of spoken language. Our results suggest that auditory thresholds of the last common ancestor of Homo and Pan were already compatible with speech reception as observed in humans. Therefore, it seems unlikely that the morphological evolution observed in the bony auditory region of fossil hominins was driven by the emergence of spoken language. Instead, the peculiar human configuration may be a by-product of morpho-functional constraints linked to brain expansion.

Transcript Isoform Diversity of Ampliconic Genes on the Y Chromosome of Great Apes.

Y chromosomal ampliconic genes (YAGs) are important for male fertility, as they encode proteins functioning in spermatogenesis. The variation in copy number and expression levels of these multicopy gene families has been studied in great apes; however, the diversity of splicing variants remains unexplored. Here, we deciphered the sequences of polyadenylated transcripts of all nine YAG families (BPY2, CDY, DAZ, HSFY, PRY, RBMY, TSPY, VCY, and XKRY) from testis samples of six great ape species (human, chimpanzee, bonobo, gorilla, Bornean orangutan, and Sumatran orangutan). To achieve this, we enriched YAG transcripts with capture probe hybridization and sequenced them with long (Pacific Biosciences) reads. Our analysis of this data set resulted in several findings. First, we observed evolutionarily conserved alternative splicing patterns for most YAG families except for BPY2 and PRY. Second, our results suggest that BPY2 transcripts and proteins originate from separate genomic regions in bonobo versus human, which is possibly facilitated by acquiring new promoters. Third, our analysis indicates that the PRY gene family, having the highest representation of noncoding transcripts, has been undergoing pseudogenization. Fourth, we have not detected signatures of selection in the five YAG families shared among great apes, even though we identified many species-specific protein-coding transcripts. Fifth, we predicted consensus disorder regions across most gene families and species, which could be used for future investigations of male infertility. Overall, our work illuminates the YAG isoform landscape and provides a genomic resource for future functional studies focusing on infertility phenotypes in humans and critically endangered great apes.