Great Ape Species Research Articles

Exonization of the LTR transposable elements in human genome.

BackgroundRetrotransposons have been shown to contribute to evolution of both structure and regulation of protein coding genes. It has been postulated that the primary mechanism by which retrotransposons contribute to structural gene evolution is through insertion into an intron or a gene flanking region, and subsequent incorporation into an exon.ResultsWe found that Long Terminal Repeat (LTR) retrotransposons are associated with 1,057 human genes (5.8%). In 256 cases LTR retrotransposons were observed in protein-coding regions, while 50 distinct protein coding exons in 45 genes were comprised exclusively of LTR RetroTransposon Sequence (LRTS). We go on to reconstruct the evolutionary history of an alternatively spliced exon of the Interleukin 22 receptor, alpha 2 gene (IL22RA2) derived from a sequence of retrotransposon of the Mammalian apparent LTR retrotransposons (MaLR) family. Sequencing and analysis of the homologous regions of genomes of several primates indicate that the LTR retrotransposon was inserted into the IL22RA2 gene at least prior to the divergence of Apes and Old World monkeys from a common ancestor (~25 MYA). We hypothesize that the recruitment of the part of LTR as a novel exon in great ape species occurred prior to the divergence of orangutans and humans from a common ancestor (~14 MYA) as a result of a single mutation in the proto-splice site.ConclusionOur analysis of LRTS exonization events has shown that the patterns of LRTS distribution in human exons support the hypothesis that LRTS played a significant role in human gene evolution by providing cis-regulatory sequences; direct incorporation of LTR sequences into protein coding regions was observed less frequently. Combination of computational and experimental approaches used for tracing the history of the LTR exonization process of IL22RA2 gene presents a promising strategy that could facilitate further studies of transposon initiated gene evolution.

A new species of great ape from the late Miocene epoch in Ethiopia

With the discovery of Ardipithecus, Orrorin and Sahelanthropus, our knowledge of hominid evolution before the emergence of Pliocene species of Australopithecus has significantly increased, extending the hominid fossil record back to at least 6 million years (Myr) ago. However, because of the dearth of fossil hominoid remains in sub-Saharan Africa spanning the period 12-7 Myr ago, nothing is known of the actual timing and mode of divergence of the African ape and hominid lineages. Most genomic-based studies suggest a late divergence date-5-6 Myr ago and 6-8 Myr ago for the human-chimp and human-gorilla splits, respectively-and some palaeontological and molecular analyses hypothesize a Eurasian origin of the African ape and hominid clade. We report here the discovery and recognition of a new species of great ape, Chororapithecus abyssinicus, from the 10-10.5-Myr-old deposits of the Chorora Formation at the southern margin of the Afar rift. To the best of our knowledge, these are the first fossils of a large-bodied Miocene ape from the African continent north of Kenya. They exhibit a gorilla-sized dentition that combines distinct shearing crests with thick enamel on its 'functional' side cusps. Visualization of the enamel-dentine junction by micro-computed tomography reveals shearing crest features that partly resemble the modern gorilla condition. These features represent genetically based structural modifications probably associated with an initial adaptation to a comparatively fibrous diet. The relatively flat cuspal enamel-dentine junction and thick enamel, however, suggest a concurrent adaptation to hard and/or abrasive food items. The combined evidence suggests that Chororapithecus may be a basal member of the gorilla clade, and that the latter exhibited some amount of adaptive and phyletic diversity at around 10-11 Myr ago.

Do bowerbirds exhibit cultures?

Definitions of what features constitute cultural behaviour, and hence define cultures are numerous. Many seem designed to describe those aspects of human behaviour which set us apart from other animals. A broad definition prescribing that the behaviour is: learned; learned socially; normative and collective is considered to apply to several species of great ape. In this paper, I review observations and experiments covering a suite of different behavioural characteristics displayed in members of the bowerbird family (Ptilonorhynchidae) and ask whether they fulfil these criteria. These include vocalisations, bower design, decoration use, bower orientation and display movements. Such a range of behaviours refutes the suggestion that these species are "one-trick ponies"--a criticism that is often levelled at claims for culture in non-primate species. I suggest that, despite a paucity of data in comparison with primate studies, it could be argued that bowerbirds may be considered to fulfil the same criteria on which we base our use of the term culture when applied to our close relatives, the great apes. If bowerbirds do have cultures, then their unusual natural history makes them a highly tractable system in which questions of social learning and culture can be tackled.

Behavioral cues that great apes use to forage for hidden food

We conducted three studies to examine whether the four great ape species (chimpanzees, bonobos, gorillas, and orangutans) are able to use behavioral experimenter-given cues in an object-choice task. In the subsequent experimental conditions subjects were presented with two eggs, one of which contained food and the other did not. In Study 1 the experimenter examined both eggs by smelling or shaking them, but only made a failed attempt to open (via biting) the egg containing food. In a control condition, the experimenter examined and attempted to open both eggs, but in reverse order to control for stimulus enhancement. The apes significantly preferred the egg that was first examined and then bitten, but had no preference in a baseline condition in which there were no cues. In Study 2, we investigated whether the apes could extend this ability to cues not observed in apes so far (i.e., attempting to pull apart the egg), as well as whether they made this discrimination based on the function of the action the experimenter performed. Subjects significantly preferred eggs presented with this novel cue, but did not prefer eggs presented with a novel but functionally irrelevant action. In Study 3, apes did not interpret human actions as cues to food-location when they already knew that the eggs were empty. Thus, great apes were able to use a variety of experimenter-given cues associated with foraging actions to locate hidden food and thereby were partially sensitive to the general purpose underlying these actions.

Ape metaphysics: Object individuation without language

Developmental research suggests that whereas very young infants individuate objects purely on spatiotemporal grounds, from (at latest) around 1 year of age children are capable of individuating objects according to the kind they belong to and the properties they instantiate. As the latter ability has been found to correlate with language, some have speculated whether it might be essentially language dependent and therefore uniquely human. Existing studies with non-human primates seem to speak against this hypothesis, but fail to present conclusive evidence due to methodological shortcomings. In the present experiments we set out to test non-linguistic object individuation in three great ape species with a refined manual search methodology. Experiment 1 tested for spatiotemporal object individuation: Subjects saw 1 or 2 objects simultaneously being placed inside a box in which they could reach, and then in both conditions only found 1 object. After retrieval of the 1 object, subjects reached again significantly more often when they had seen 2 than when they had seen 1 object. Experiment 2 tested for object individuation according to property/kind information only: Subjects saw 1 object being placed inside the box, and then either found that object (expected) or an object of a different kind (unexpected). Analogously to Experiment 1, after retrieval of the 1 object, subjects reached again significantly more often in the unexpected than in the expected condition. These results thus confirm previous findings suggesting that individuating objects according to their property/kind is neither uniquely human nor essentially language dependent. It remains to be seen, however, whether this kind of object individuation requires sortal concepts as human linguistic thinkers use them, or whether some simpler form of tracking properties is sufficient.

Culture in great apes: using intricate complexity in feeding skills to trace the evolutionary origin of human technical prowess.

Geographical cataloguing of traits, as used in human ethnography, has led to the description of 'culture' in some non-human great apes. Culture, in these terms, is detected as a pattern of local ignorance resulting from environmental constraints on knowledge transmission. However, in many cases, the geographical variations may alternatively be explained by ecology. Social transmission of information can reliably be identified in many other animal species, by experiment or distinctive patterns in distribution; but the excitement of detecting culture in great apes derives from the possibility of understanding the evolution of cumulative technological culture in humans. Given this interest, I argue that great ape research should concentrate on technically complex behaviour patterns that are ubiquitous within a local population; in these cases, a wholly non-social ontogeny is highly unlikely. From this perspective, cultural transmission has an important role in the elaborate feeding skills of all species of great ape, in conveying the 'gist' or organization of skills. In contrast, social learning is unlikely to be responsible for local stylistic differences, which are apt to reflect sensitive adaptations to ecology.

Push or Pull: Imitation vs. Emulation in Great Apes and Human Children

AbstractAll four species of great apes and young human children (12–24 mo of age) were administered an imitation task designed to distinguish between results learning (emulation) and action learning (imitation). Some subjects were exposed to a demonstrator either pushing or pulling a door to open a box, whereas others simply saw the door of the box opening itself in one of the two directions (the ghost control). Most of the apes successfully opened the box in both experimental conditions, as well as in a baseline condition, but without being influenced either by the demonstrator's actions or by the door's motions. In contrast, human children over 12 mo of age were influenced by the demonstration: the 18‐mo‐olds were influenced by the demonstrator's actions, and the 24‐mo‐olds were influenced both by the demonstrator's actions and by the door's motions in the ghost control. These results provide support for the hypothesis that human children have a greater propensity than great apes for focusing either on a demonstrator's action or on the result of their action, as needed, in social learning situations.

Are apes really inequity averse?

Brosnan et al. (Brosnan, S. F. Schiff, H. C. & de Waal, F. B. M. 2005 Tolerance for inequity may increase with social closeness in chimpanzees. Proc. R. Soc. B272, 253-258) found that chimpanzees showed increased levels of rejection for less-preferred food when competitors received better food than themselves and postulated as an explanation inequity aversion. In the present study, we extended these findings by adding important control conditions, and we investigated whether inequity aversion could also be found in the other great ape species and whether it would be influenced by subjects' relationship with the competitor. In the present study, subjects showed a pattern of food rejection opposite to the subjects of the above study by Brosnan et al. (2005). Our apes ignored fewer food pieces and stayed longer in front of the experimenter when a conspecific received better food than themselves. Moreover, chimpanzees begged more vigorously when the conspecific got favoured food. The most plausible explanation for these results is the food expectation hypothesis - seeing another individual receive high-quality food creates the expectation of receiving the same food oneself - and not inequity aversion.

Apes Save Tools for Future Use

Planning for future needs, not just current ones, is one of the most formidable human cognitive achievements. Whether this skill is a uniquely human adaptation is a controversial issue. In a study we conducted, bonobos and orangutans selected, transported, and saved appropriate tools above baseline levels to use them 1 hour later (experiment 1). Experiment 2 extended these results to a 14-hour delay between collecting and using the tools. Experiment 3 showed that seeing the apparatus during tool selection was not necessary to succeed. These findings suggest that the precursor skills for planning for the future evolved in great apes before 14 million years ago, when all extant great ape species shared a common ancestor.

A preliminary comparative analysis of primate segmental duplications shows elevated substitution rates and a great-ape expansion of intrachromosomal duplications

Compared with other sequenced animal genomes, human segmental duplications appear larger, more interspersed, and disproportionately represented as high-sequence identity alignments. Global sequence divergence estimates of human duplications have suggested an expansion relatively recently during hominoid evolution. Based on primate comparative sequence analysis of 37 unique duplication-transition regions, we establish a molecular clock for their divergence that shows a significant increase in their effective substitution rate when compared with unique genomic sequence. Fluorescent in situ hybridization (FISH) analyses from 1053 random nonhuman primate BACs indicate that great-ape species have been enriched for interspersed segmental duplications compared with representative Old World and New World monkeys. These findings support computational analyses that show a 12-fold excess of recent (>98%) intrachromosomal duplications when compared with duplications between nonhomologous chromosomes. These architectural shifts in genomic structure and elevated substitution rates have important implications for the emergence of new genes, gene-expression differences, and structural variation among humans and great apes.

A Universal Microsatellite Multiplex Kit for Genetic Analysis of Great Apes

DNA profiling with microsatellite markers is a commonly used genetic method of studying the great apes. An efficient method of generating the genetic data is amplification of multiple microsatellites in a single PCR reaction. Here we describe a PCR multiplex in which 9 genetic markers can be amplified simultaneously, thereby saving time, expenses and DNA. This marker system can discriminate between all the great ape species except bonobos and chimpanzees. Furthermore, the cumulative probability of identity values were low for all 4 species tested.

Gestural communication of orangutans (Pongo pygmaeus)

This study represents a systematic investigation of the communicative repertoire of Sumatran orangutans ( Pongo pygmaeus abelii ), with a focus on intentional signals in two groups of captive orangutans. The goal was to analyze the signal repertoire with respect to (1) the number and frequency of signals (gestures, facial expressions, and actions), (2) the variability of individual repertoires as a function of group, age class, and sex, and (3) the flexibility of use in terms of 'means-end dissociation' and 'audience effects' and to interpret the findings in terms of the ecology, social structure and socio-cognitive skills of orangutans. The results show that orangutans use a remarkable number of signals including tactile and visual gestures as well as several more complex actions, though few facial expressions and no auditory gestures were observed. One third of signals were used within a play context, followed by one fourth of interactions in the context of ingestion. Although the repertoire included several visual gestures, most of the signals produced were tactile gestures and they were used particularly in the contexts of affiliation and agonism, whereas visual gestures dominated in the context of grooming, ingestion and sexual behavior. Individual repertoires showed a remarkable degree of variability as a function of age and group affiliation. Orangutans used their signals flexibly in several functional contexts and adjusted the signal they used depending on the attentional state of the recipient, similar to findings of other great ape species and gibbons. Thus, the communicative behavior of orangutans is characterized by a variable and flexible use of signals possibly reflecting their highly variable social structure and their sophisticated socio-cognitive skills, with the dominance of tactile gestures corresponding to the arboreal nature of this species.

Neandertals

Neandertals

World atlas of great apes and their conservation

Despite the dedicated efforts of many individuals and organizations, the great apes—our closest living relatives—are on the very edge of extinction. This sweeping atlas provides a comprehensive overview of what is currently known about all six species of great apes—chimpanzee, bonobo, Sumatran orangutan, Bornean orangutan, eastern gorilla, and western lowland gorilla. Created in association with The Great Apes Survival Project (GRASP), this book gives a thorough background on ape behavior and ecology for each species, including detailed habitat requirements, the apes' ecological role, and the possible consequences of their decline. World Atlas of Great Apes also offers a full description of the threats, current conservation efforts, and additional protection needed for each species across its entire range. Many full-color maps and illustrations make the abundance of information accessible to a broad readership, from specialists and policymakers to general readers concerned about the survival of these charismatic primates.

Who's afraid of Homo sapiens?

Understanding how humans differ from other animals, as well as how we are like them, requires comparative investigations. For the purpose of documenting the distinctive features of humans, the most informative research involves comparing humans to our closest relatives–the chimpanzees and other great apes. Psychology and anthropology have maintained a tradition of empirical comparative research on human specializations of cognition. The neurosciences, by contrast, have been dominated by the model-animal research paradigm, which presupposes the commonality of "basic" features of brain organization across species and discourages serious treatment of species differences. As a result, the neurosciences have made little progress in understanding human brain specializations. Recent developments in neuroimaging, genomics, and other non-invasive techniques make it possible to directly compare humans and nonhuman species at levels of organization that were previously inaccessible, offering the hope of gaining a better understanding of the species-specific features of the human brain. This hope will be dashed, however, if chimpanzees and other great ape species become unavailable for even non-invasive research.

How the great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) perform on the reversed contingency task: The effects of food quantity and food visibility.

S. T. Boysen and G. G. Berntson (1995) found that chimpanzees performed poorly on a reversed contingency task in which they had to point to the smaller of 2 food quantities to acquire the larger quantity. The authors compared the performance of 4 great ape species (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) on the reversed contingency task while manipulating food quantity (0-4 or 1-4) and food visibility (visible pairs or covered pairs). Results showed no systematic species differences but large individual differences. Some individuals of each species were able to solve the reversed contingency task. Both quantity and visibility of the food items had a significant effect on performance. Subjects performed better when the disparity between quantities was smaller and the quantities were not directly visible.

The Rise and Fall of the Chemoattractant Receptor GPR33

Chemokine and chemoattractant receptors are members of the large superfamily of G protein-coupled receptors (GPCR), which control leukocyte chemotaxis. In addition to their physiological role, several chemokine and chemoattractant receptors, such as CCR5 and Duffy, have been directly associated with pathogen entry. GPR33 is an orphan chemoattractant GPCR that was previously identified as a pseudogene in humans. GPR33 evolved in mammals about 125-190 million years ago. The cloning and analysis of more than 120 mammalian GPR33 orthologs from 16 of 18 eutherian orders revealed an inactivation of this chemoattractant GPCR not only in humans, but also in several great ape and rodent species. Intriguingly, in all ape and some rodent species where the inactivation occurred, samples harbored both pseudogene and intact gene variants. The analysis of over 1200 human individuals representing all major linguistic groups revealed that the intact allele of GPR33 is still present in the human population. Estimates of the age of the human alleles suggest inactivation in the past 1 million years. Similarly, analysis of more than 120 wild-caught gray rats (Rattus norvegicus), revealed that inactivation of gpr33 is worldwide fixed and occurred in less than 0.7 million years ago. The coincidental inactivation and its fixation in several species of distantly related mammalian orders suggest a selective pressure on this chemoattractant receptor gene.

Neural connectivity and cortical substrates of cognition in hominoids

Cognitive functions and information processing recruit discrete neural systems in the cortex and white matter. We tested the idea that specific regions in the cerebrum are differentially enlarged in humans and that some of the neural reorganizational events that took place during hominoid evolution were species-specific and independent of changes in absolute brain size. We used magnetic resonance images of the living brains of 10 human and 17 ape subjects to obtain volumetric estimates of regions of interest. We parcellated the white matter in the frontal and temporal lobes into two sectors, including the white matter immediately underlying the cortex (gyral white matter) and the rest of white matter (core). We outlined the dorsal, mesial, and orbital subdivisions of the frontal lobe and analyzed the relationship between cortex and gyral white matter within each subdivision. For all regions analyzed, the observed human values are as large as expected, with the exception of the gyral white matter, which is larger than expected in humans. We found that orangutans had a relatively smaller orbital sector than any other great ape species, with no overlap in individual values. We found that the relative size of the dorsal subdivision is larger in chimpanzees than in bonobos, and that the ratio of gyral white matter to cortex stands out in Pan in comparison to Gorilla and Pongo. Individual variability, possible sex differences, and hemispheric asymmetries were present not only in humans, but in apes as well. Differences in the distribution of neural connectivity and cortical sectors were identified among great ape species that share similar absolute brain sizes. Given that these regions are part of neural systems with distinct functional attributes, we suggest that the observed differences may reflect different evolutionary pressures on regulatory mechanisms of complex cognitive functions, including social cognition.

Use of space in a non-naturalistic environment by chimpanzees ( Pan troglodytes) and lowland gorillas ( Gorilla gorilla gorilla)

Chimpanzees and gorillas are the two most common species of great ape in captive facilities in North America. This study examined patterns of space use by 14 gorillas and six chimpanzees housed in similar non-naturalistic environments at Lincoln Park Zoo in Chicago, IL. The location of each individual was recorded in relation to elements of the environment over a two-year period. These data were compared to volumetric measurements of the enclosures to determine “preferences” for particular environmental elements. Chimpanzees preferred the highest tier of the enclosure and the gorillas preferred the floor level. Both species showed preferences for doorways, corners and the mesh barriers adjacent to keeper areas. These data supplement data from wild populations of apes and provide information useful for those seeking to design new ape enclosures or renovate existing facilities.

Evolution versus constitution: differences in chromosomal inversion

We compared the chromosomal breakpoints of evolutionary conserved and constitutional inversions. Multicolor banding and human-specific bacterial artificial chromosomes were applied to map the breakpoints of constitutional pericentric inversions on human chromosomes 2 and 9. For the first time, we present a high-resolution analysis of the breakpoint regions, which are characterized by gene destitution, co-localization with fragile sites, multitude repeats as well as pseudogenes and, remarkably, a large sequence homology to the opposite breakpoint. In contrast, evolutionary inversion breakpoints lack such extensive cross-hybridizing regions and are often associated with fragile sites of the genome and low-copy repeats. These molecular characteristics gave evidence for different types of inversion formation and indicate that evolutionary inversions cannot originate from constitutional inversions like those of chromosomes 2 and 9. Finally, the constitutional inversion breakpoints were investigated on three different great ape species and on four test persons each bearing the same cytogenetically determined inversion on chromosomes 2 and 9, respectively. Our data indicate the existence of different molecular breakpoints for the two variant chromosomes.