Genetic signature of anthropogenic population collapse in orang-utans.
ABSTRACT: Great ape populations are undergoing a dramatic decline, which is predicted to result in their extinction in the wild from entire regions in the near future. Recent findings have particularly focused on African apes, and have implicated multiple factors contributing to this decline, such as deforestation, hunting, and disease. Less well-publicised, but equally dramatic, has been the decline in orang-utans, whose distribution is limited to parts of Sumatra and Borneo. Using the largest-ever genetic sample from wild orang-utan populations, we show strong evidence for a recent demographic collapse in North Eastern Borneo and demonstrate that this signature is independent of the mutation and demographic models used. This is the first demonstration that genetic data can detect and quantify the effect of recent, human-induced deforestation and habitat fragmentation on an endangered species. Because current demographic collapses are usually confounded by ancient events, this suggests a much more dramatic decline than demographic data alone and emphasises the need for major conservation efforts.
Project description:Bornean orang-utans experienced a major demographic decline and local extirpations during the Pleistocene and Holocene due to climate change, the arrival of modern humans, of farmers and recent commercially-driven habitat loss and fragmentation. The recent loss of habitat and its dramatic fragmentation has affected the patterns of genetic variability and differentiation among the remaining populations and increased the extinction risk of the most isolated ones. However, the contribution of recent demographic events to such genetic patterns is still not fully clear. Indeed, it can be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric demographic events. Here, we investigated the genetic structure and population size dynamics of orang-utans from different sites. Altogether 126 individuals were analyzed and a full-likelihood Bayesian approach was applied. All sites exhibited clear signals of population decline. Population structure is known to generate spurious bottleneck signals and we found that it does indeed contribute to the signals observed. However, population structure alone does not easily explain the observed patterns. The dating of the population decline varied across sites but was always within the 200-2000 years period. This suggests that in some sites at least, orang-utan populations were affected by demographic events that started before the recent anthropogenic effects that occurred in Borneo. These results do not mean that the recent forest exploitation did not leave its genetic mark on orang-utans but suggests that the genetic pool of orang-utans is also impacted by more ancient events. While we cannot identify the main cause for this decline, our results suggests that the decline may be related to the arrival of the first farmers or climatic events, and that more theoretical work is needed to understand how multiple demographic events impact the genome of species and how we can assess their relative contributions.
Project description:The conversion of forest to agriculture continues to contribute to the loss and fragmentation of remaining orang-utan habitat. There are still few published estimates of orang-utan densities in these heavily modified agricultural areas to inform range-wide population assessments and conservation strategies. In addition, little is known about what landscape features promote orang-utan habitat use. Using indirect nest count methods, we implemented surveys and estimated population densities of the Northeast Bornean orang-utan (Pongo pygmaeus morio) across the continuous logged forest and forest remnants in a recently salvage-logged area and oil palm plantations in Sabah, Malaysian Borneo. We then assessed the influence of landscape features and forest structural metrics obtained from LiDAR data on estimates of orang-utan density. Recent salvage logging appeared to have a little short-term effect on orang-utan density (2.35?ind/km 2 ), which remained similar to recovering logged forest nearby (2.32?ind/km 2 ). Orang-utans were also present in remnant forest patches in oil palm plantations, but at significantly lower numbers (0.82?ind/km 2 ) than nearby logged forest and salvage-logged areas. Densities were strongly influenced by variation in canopy height but were not associated with other potential covariates. Our findings suggest that orang-utans currently exist, at least in the short-term, within human-modified landscapes, providing that remnant forest patches remain. We urge greater recognition of the role that these degraded habitats can have in supporting orang-utan populations, and that future range-wide analyses and conservation strategies better incorporate data from human-modified landscapes.
Project description:Confiscated and displaced mammals are often taken to sanctuaries, where the explicit goal may be reintroduction to the wild. By inadvertently collecting animals from different source populations, however, such efforts risk reintroducing individuals that have not been in genetic contact for significant periods of time. Using genetic analyses and 44 years of data from Camp Leakey, an orang-utan rehabilitation site on Borneo, we determined the minimum extent to which orang-utans representing non-native, geographically and reproductively isolated taxa were reintroduced into the surrounding wild population. We found two reintroduced females were from a non-native subspecies, and have since produced at least 22 hybridized and introgressed descendants to date, of which at least 15 are living. Given that Bornean orang-utan subspecies are thought to have diverged from a common ancestor around 176,000 years ago, with marked differentiation over the last 80,000 years, we highlight the need for further evaluation of the effects of hybridizing orang-utans of different taxa--particularly in light of the ~1500 displaced orang-utans awaiting urgent reintroduction. As endangered mammals are increasing in number in sanctuaries worldwide, we stress the need for re-examination of historical reintroductions, to assess the extent and effects of de facto translocations in the past.
Project description:Transfers and services are frequent in the animal kingdom. However, there is no clear evidence in animals that such transactions are based on weighing costs and benefits when giving or returning favours and keeping track of them over time (i.e. calculated reciprocity). We tested two orang-utans (Pongo pygmaeus abelii) in a token-exchange paradigm, in which each individual could exchange a token for food with the experimenter but only after first obtaining the token from the other orang-utan. Each orang-utan possessed tokens valuable to their partner but useless to themselves. Both orang-utans actively transferred numerous tokens (mostly partner-valuable) to their partner. One of the orang-utans routinely used gestures to request tokens while the other complied with such requests. Although initially the transfers were biased in one direction, they became more balanced towards the end of the study. Indeed, data on the last three series produced evidence of reciprocity both between and within trials. We observed an increase in the number and complexity of exchanges and alternations. This study is the first experimental demonstration of the occurrence of direct transfers of goods based on calculated reciprocity in non-human-primates.
Project description:To gain insights into evolutionary forces that have shaped the history of Bornean and Sumatran populations of orang-utans, we compare patterns of variation across more than 11 million single nucleotide polymorphisms found by previous mitochondrial and autosomal genome sequencing of 10 wild-caught orang-utans. Our analysis of the mitochondrial data yields a far more ancient split time between the two populations (~3.4 million years ago) than estimates based on autosomal data (0.4 million years ago), suggesting a complex speciation process with moderate levels of primarily male migration. We find that the distribution of selection coefficients consistent with the observed frequency spectrum of autosomal non-synonymous polymorphisms in orang-utans is similar to the distribution in humans. Our analysis indicates that 35% of genes have evolved under detectable negative selection. Overall, our findings suggest that purifying natural selection, genetic drift, and a complex demographic history are the dominant drivers of genome evolution for the two orang-utan populations.
Project description:The integration of Bayesian analysis into existing great ape survey methods could be used to generate precise and reliable population estimates of Bornean orang-utans. We used the Marked Nest Count (MNC) method to count new orang-utan nests at seven previously undocumented study sites in Sarawak, Malaysia. Our survey teams marked new nests on the first survey and revisited the plots on two more occasions; after about 21 and 42 days respectively. We used the N-mixture models to integrate suitability, abundance and detection models which account for zero inflation and imperfect detection for the analysis. The result was a combined estimate of 355 orang-utans with the 95% highest density interval (HDI) of 135 to 602 individuals. We visually inspected the posterior distributions of our parameters and compared precisions between study sites. We subsequently assess the strength or reliability of the generated estimates using identifiability tests. Only three out of the seven estimates had <35% overlap to indicate strong reliability. We discussed the limitations and advantages of our study design, and made recommendations to improve the sampling scheme. Over the course of this research, two of the study sites were gazetted as extensions to the Lanjak-Entimau Wildlife Sanctuary for orang-utan conservation.
Project description:<h4>Background</h4>Several studies suggested great ape cultures, arguing that human cumulative culture presumably evolved from such a foundation. These focused on conspicuous behaviours, and showed rich geographic variation, which could not be attributed to known ecological or genetic differences. Although geographic variation within call types (accents) has previously been reported for orang-utans and other primate species, we examine geographic variation in the presence/absence of discrete call types (dialects). Because orang-utans have been shown to have geographic variation that is not completely explicable by genetic or ecological factors we hypothesized that this will be similar in the call domain and predict that discrete call type variation between populations will be found.<h4>Methodology/principal findings</h4>We examined long-term behavioural data from five orang-utan populations and collected fecal samples for genetic analyses. We show that there is geographic variation in the presence of discrete types of calls. In exactly the same behavioural context (nest building and infant retrieval), individuals in different wild populations customarily emit either qualitatively different calls or calls in some but not in others. By comparing patterns in call-type and genetic similarity, we suggest that the observed variation is not likely to be explained by genetic or ecological differences.<h4>Conclusion/significance</h4>These results are consistent with the potential presence of 'call cultures' and suggest that wild orang-utans possess the ability to invent arbitrary calls, which spread through social learning. These findings differ substantially from those that have been reported for primates before. First, the results reported here are on dialect and not on accent. Second, this study presents cases of production learning whereas most primate studies on vocal learning were cases of contextual learning. We conclude with speculating on how these findings might assist in bridging the gap between vocal communication in non-human primates and human speech.
Project description:'Orang-utan' is derived from a Malay term meaning 'man of the forest' and aptly describes the southeast Asian great apes native to Sumatra and Borneo. The orang-utan species, Pongo abelii (Sumatran) and Pongo pygmaeus (Bornean), are the most phylogenetically distant great apes from humans, thereby providing an informative perspective on hominid evolution. Here we present a Sumatran orang-utan draft genome assembly and short read sequence data from five Sumatran and five Bornean orang-utan genomes. Our analyses reveal that, compared to other primates, the orang-utan genome has many unique features. Structural evolution of the orang-utan genome has proceeded much more slowly than other great apes, evidenced by fewer rearrangements, less segmental duplication, a lower rate of gene family turnover and surprisingly quiescent Alu repeats, which have played a major role in restructuring other primate genomes. We also describe a primate polymorphic neocentromere, found in both Pongo species, emphasizing the gradual evolution of orang-utan genome structure. Orang-utans have extremely low energy usage for a eutherian mammal, far lower than their hominid relatives. Adding their genome to the repertoire of sequenced primates illuminates new signals of positive selection in several pathways including glycolipid metabolism. From the population perspective, both Pongo species are deeply diverse; however, Sumatran individuals possess greater diversity than their Bornean counterparts, and more species-specific variation. Our estimate of Bornean/Sumatran speciation time, 400,000?years ago, is more recent than most previous studies and underscores the complexity of the orang-utan speciation process. Despite a smaller modern census population size, the Sumatran effective population size (N(e)) expanded exponentially relative to the ancestral N(e) after the split, while Bornean N(e) declined over the same period. Overall, the resources and analyses presented here offer new opportunities in evolutionary genomics, insights into hominid biology, and an extensive database of variation for conservation efforts.
Project description:Orang-utans played a communication game in two studies testing their ability to produce and comprehend requestive pointing. While the 'communicator' could see but not obtain hidden food, the 'donor' could release the food to the communicator, but could not see its location for herself. They could coordinate successfully if the communicator pointed to the food, and if the donor comprehended his communicative goal and responded pro-socially. In Study 1, one orang-utan pointed regularly and accurately for peers. However, they responded only rarely. In Study 2, a human experimenter played the communicator's role in three conditions, testing the apes' comprehension of points of different heights and different degrees of ostension. There was no effect of condition. However, across conditions one donor performed well individually, and as a group orang-utans' comprehension performance tended towards significance. We explain this on the grounds that comprehension required inferences that they found difficult - but not impossible. The finding has valuable implications for our thinking about the development of pointing in phylogeny.
Project description:The hypervariable region I (HVRI) is persistently used to discern haplotypes, to distinguish geographic subpopulations, and to infer taxonomy in a range of organisms. Numerous studies have highlighted greater heterogeneity elsewhere in the mitochondrial DNA control region, however-particularly, in some species, in other understudied hypervariable regions. To assess the abundance and utility of such potential variations in orang-utans, we characterised 36 complete control-region haplotypes, of which 13 were of Sumatran and 23 of Bornean maternal ancestry, and compared polymorphisms within these and within shorter HVRI segments predominantly analysed in prior phylogenetic studies of Sumatran (~385 bp) and Bornean (~323 bp) orang-utans. We amplified the complete control region in a single PCR that proved successful even with highly degraded, non-invasive samples. By using species-specific primers to produce a single large amplicon (~1600 bp) comprising flanking coding regions, our method also serves to better avoid amplification of nuclear mitochondrial insertions (numts). We found the number, length and position of hypervariable regions is inconsistent between orang-utan species, and that prior definitions of the HVRI were haphazard. Polymorphisms occurring outside the predominantly analysed segments were phylogeographically informative in isolation, and could be used to assign haplotypes to comparable clades concordant with geographic subpopulations. The predominantly analysed segments could discern only up to 76% of all haplotypes, highlighting the forensic utility of complete control-region sequences. In the face of declining sequencing costs and our proven application to poor-quality DNA extracts, we see no reason to ever amplify only specific 'hypervariable regions' in any taxa, particularly as their lengths and positions are inconsistent and cannot be reliably defined-yet this strategy predominates widely. Given their greater utility and consistency, we instead advocate analysis of complete control-region sequences in future studies, where any shorter segment might otherwise have proven the region of choice.