With fewer than 800 individuals, P. tapanuliensis is among the most endangered great apes

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos []. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids []. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 []. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive.

The mitochondrial DNA molecule of Sumatran orangutan and a molecular proposal for two (Bornean and Sumatran) species of orangutan.

This published work and the nomenclatural acts it contains have been registered in ZooBank ( http://zoobank.org/ ), the online registration system for the International Commission on Zoological Nomenclature (ICZN). The LSID (Life Science Identifier) for this publication is urn:lsid:zoobank.org:pub:68FBFE28-103C-4E95-89BD-974A70D026F7.

Pongo tapanuliensis occurs only in a small number of forest fragments in the districts of Central, North, and South Tapanuli, Indonesia ( Figure 1 A). The total distribution covers approximately 1,000 km, with an estimated population size of fewer than 800 individuals []. The current distribution of P. tapanuliensis is almost completely restricted to medium elevation hill and submontane forest (∼300–1,300 m above sea level) []. Although densities are highest in primary forest, it does occur at lower densities in mixed agroforest at the edge of primary forest areas []. Until relatively recently, P. tapanuliensis was more widespread to the south and west of the current distribution, although evidence for this is largely anecdotal [].

A Survey of Some Forested Areas in South and Central Tapanuli, North Sumatra: New Chances for Orangutan Conservation.

The external morphology of P. tapanuliensis is more similar to that of P. abelii in its linear body build and more cinnamon pelage than that of P. pygmaeus. The hair texture of P. tapanuliensis is frizzier, contrasting in particular with the long, loose body hair of P. abelii. Pongo tapanuliensis has a prominent moustache and flat flanges covered in downy hair in dominant males, whereas flanges of older males resemble more those of Bornean males. Females of P. tapanuliensis have beards, unlike those of P. pygmaeus.

Craniometrically, the type skull of P. tapanuliensis ( Figure 1 B) is significantly smaller than any skull of comparable developmental stage of other orangutans; it falls outside of the interquartile ranges of P. abelii and P. pygmaeus for 24 of 39 cranio-mandibular measurements ( Table S1 ). A principal-component analysis (PCA) of 26 cranio-mandibular measurements commonly used in primate taxonomic classification [] shows consistent differences between P. tapanuliensis and the two currently recognized species ( Figures 1 C and S2 ).

(C) Violin plots of the first seven principal components of 26 cranio-mandibular morphological variables of eight north Sumatran P. abelii and 19 Bornean P. pygmaeus individuals of similar developmental state as the P. tapanuliensis holotype skull (black horizontal lines). See also Figure S2

(B) Holotype skull and mandible of P. tapanuliensis from a recently deceased individual from Batang Toru. See also Figure S1 and Tables S1 and S2

(A) Current distribution of Pongo tapanuliensis on Sumatra. The holotype locality is marked with a red star. The area shown in the map is indicated in Figure 2 A.

Pongo tapanuliensis differs specifically from Pongo “pygmaeus” palaeosumatrensis in the smaller size of the first upper molar (mesio-distal length 13.7 versus >14.0 mm, buccolingual breadth 11.4 versus >12.1 mm, crown area 155.2 versus >175.5 mm Figure S1 ).

Pongo tapanuliensis differs from P. pygmaeus by possessing a nearly straight zygomaxillary suture and lower orbit (orbit height 33.4 versus >35.3 mm); the male long call has a longer duration (>111 versus <90 s) with a greater number of pulses (>52 versus <45 pulses), and is delivered at a greater rate (>0.82 versus <0.79 pulses per 20 s).

Pongo tapanuliensis differs specifically from P. abelii by its deep suborbital fossa, triangular pyriform aperture, and angled facial profile; the longer nuchal surface (70.5 versus <64.7 mm); the wider rostrum, posterior to the canines (59.9 versus <59 mm); the narrower orbits (33.8 versus <34.6 mm); the shorter (29.2 versus >30.0 mm) and narrower (23.2 versus >23.3 mm) foramen magnum; the narrower bicondylar breadth (120.0 versus >127.2 mm); the narrower mandibular incisor row (24.4 versus >28.3 mm); and the greater mesio-distal length of the upper canine (19.4 versus <17.6 mm). The male long call has a higher maximum frequency range of the roar pulse type (>800 versus <747 Hz) with a higher “shape” (>952 versus <934 Hz/s).

We compared the holotype to a comprehensive comparative dataset of 33 adult male orangutans from ten institutions housing osteological specimens. Summary statistics for all measurements are listed in Tables S1–S3 . Pongo tapanuliensis differs from all extant orangutans in the breadth of the upper canine (21.5 versus <20.9 mm), the shallow face depth (6.0 versus >8.4 mm), the narrower interpterygoid distance (at posterior end of pterygoids 33.8 versus >43.9 mm; at anterior end of pterygoids, 33.7 versus >43.0 mm), the shorter tympanic tube (23.9 versus >28.4 mm, mostly >30 mm), the shorter temporomandibular joint (22.5 versus >24.7 mm), the narrower maxillary incisor row (28.3 versus >30.1 mm), the narrower distance across the palate at the first molars (62.7 versus >65.7 mm), the shorter horizontal length of the mandibular symphysis (49.3 versus >53.7 mm), the smaller inferior transverse torus (horizontal length from anterior surface of symphysis 31.8 compared to >36.0 mm), and the width of the ascending ramus of the mandible (55.9 versus >56.3 mm).

Adult individuals of P. tapanuliensis (P2591-M435788–P2591-M435790) photographed by Tim Laman in the Batang Toru Forest Complex (1°41’9.1”N, 98°59’38.1”E), North Tapanuli District, North Sumatra, Indonesia. Paratypes are available from MorphoBank at http://morphobank.org/permalink/?P2591

The complete skeleton of an adult male orangutan that died from wounds sustained by local villagers in November 2013 near Sugi Tonga, Marancar, Tapanuli (Batang Toru) Forest Complex (1°35’54.1”N, 99°16’36.5”E), South Tapanuli District, North Sumatra, Indonesia. Skull and postcranium are lodged in the Museum Zoologicum Bogoriense, Indonesia, under accession number MZB39182 . High-resolution 3D reconstructions of the skull and mandible are available from MorphoBank, http://morphobank.org/permalink/?P2591

The species name refers to three North Sumatran districts (North, Central, and South Tapanuli) to which P. tapanuliensis is endemic.

Despite decades of field studies [], our knowledge of variation among orangutans remains limited as many populations occur in isolated and inaccessible habitats, leaving questions regarding their evolutionary history and taxonomic classification largely unresolved. In particular, Sumatran populations south of Lake Toba had long been overlooked, even though a 1939 review of the species’ range mentioned that orangutans had been reported in several forest areas in that region []. Based on diverse sources of evidence, we describe a new orangutan species, Pongo tapanuliensis, that encompasses a geographically and genetically isolated population found in the Batang Toru area at the southernmost range limit of extant Sumatran orangutans, south of Lake Toba, Indonesia.

Discussion

14 Coolidge H.J. Pan Paniscus. Pigmy chimpanzee from south of the Congo River. 5 Groves C.P.

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Shea B.T. Unfinished business: Mahalanobis and a clockwork orang. 15 Shea B.T.

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Fleagle J.G. Patterns of diversity in gorilla cranial morphology. 17 Groves C.P. A history of gorilla taxonomy. 1 Groves C.P. Primate Taxonomy. 18 Geissmann T.

Lwin N.

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Momberg F. A new species of snub-nosed monkey, genus Rhinopithecus Milne-Edwards, 1872 (Primates, Colobinae), from northern Kachin state, northeastern Myanmar. 19 Jones T.

Ehardt C.L.

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De Luca D.W. The highland mangabey Lophocebus kipunji: a new species of African monkey. 20 Li C.

Zhao C.

Fan P.F. White-cheeked macaque (Macaca leucogenys): a new macaque species from Medog, southeastern Tibet. 21 Munds R.A.

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Ford S.M. Taxonomy of the Bornean slow loris, with new species Nycticebus kayan (Primates, Lorisidae). 22 Rasoloarison R.M.

Weisrock D.W.

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Rakotondravony D.

Kappeler P.M. Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from Eastern Madagascar. 23 Svensson M.S.

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Bearder S.K. A giant among dwarfs: a new species of galago (Primates: Galagidae) from Angola. 24 Davenport T.R.B.

Stanley W.T.

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Olson L.E. A new genus of African monkey, Rungwecebus: morphology, ecology, and molecular phylogenetics. 25 Fan P.F.

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et al. Description of a new species of Hoolock gibbon (Primates: Hylobatidae) based on integrative taxonomy. Other hominoid species and subspecies were previously described using standard univariate and multivariate techniques to quantify morphological character differences. The elevation of bonobos (P. paniscus) from a subspecies to a species dates back to Coolidge [] and was based on summary statistics of primarily morphological data from a single female specimen of P. paniscus, five available P. paniscus skulls, and comparative data of what is now P. troglodytes. Groves and colleagues [] and Shea et al. [] supported Coolidge’s proposal using larger sample sizes and discriminant function analyses. Shea et al. [] remarked that the species designation for P. paniscus, which was largely based on morphological comparisons, was ultimately strengthened by genetic, ecological, and behavioral data, as we attempted here for Pongo tapanuliensis. For the genus Gorilla, Stumpf et al. [] and Groves [] used cranio-mandibular data from 747 individuals from 19 geographic regions, confirming a classification of the genus into two species (G. gorilla and G. beringei), as proposed earlier by Groves []. Other recent primate species descriptions primarily relied on an inconsistent mix of data on pelage color, ecology, morphology, and/or vocalizations [], with only a few also incorporating genetic analyses [].

26 Jost L. G ST and its relatives do not measure differentiation. 27 Whitlock M.C. G’ ST and D do not replace F ST . Figure 2 Distribution, Genomic Diversity, and Population Structure of the Genus Pongo Show full caption (A) Sampling areas across the current distribution of orangutans. The contour indicates the extent of the exposed Sunda Shelf during the Last Glacial Maximum. The black rectangle delimits the area shown in Figure 1 A. n indicates the number of sequenced individuals. See also Table S4 (B) PCA of genomic diversity in Pongo. Axis labels show the percentages of the total variance explained by the first two principal components. Colored bars in the insert represent the distribution of nucleotide diversity in genome-wide 1-Mb windows across sampling areas. (C) Bayesian clustering analysis of population structure using the program ADMIXTURE. Each vertical bar depicts an individual, with colors representing the inferred ancestry proportions with different assumed numbers of genetic clusters (K, horizontal sections). Here, we used an integrative approach by corroborating the morphological analysis and behavioral and ecological data with whole-genome data of 37 orangutans with known provenance, covering the entire range of extant orangutans including areas never sampled before ( Figure 2 A; Table S4 ). We applied a model-based approach to statistically evaluate competing demographic models, identify independent evolutionary lineages and infer levels of gene flow and the timing of genetic isolation between lineages. This enabled us to directly compare complex and realistic models of speciation. We refrained from directly comparing genetic differentiation among the three species in the genus Pongo with that of other hominoids, as we deem such comparisons problematic in order to evaluate whether P. tapanuliensis constitutes a new species. This is because estimates of genetic differentiation reflect a combination of divergence time, demographic history, and gene flow and are also influenced by the employed genetic marker system [].

28 Nater A.

Arora N.

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Singleton I.

Wich S.A.

Fredriksson G.

Perwitasari-Farajallah D.

Pamungkas J.

Krützen M. Marked population structure and recent migration in the critically endangered Sumatran orangutan (Pongo abelii). 29 Nielsen R.

Wakeley J. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. 30 Palsbøll P.J.

Bérubé M.

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Notarbartolo-Di-Sciara G.

Nielsen R. Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. A PCA ( Figure 2 B) of genomic diversity highlighted the divergence between individuals from Borneo and Sumatra (PC1) but also separated P. tapanuliensis from P. abelii (PC2). The same clustering pattern was also found in a model-based analysis of population structure ( Figure 2 C) and is consistent with an earlier genetic study analyzing a larger number of non-invasively collected samples using microsatellite markers []. However, although such clustering approaches are powerful in detecting extant population structure, population history and speciation cannot be inferred, as these methods are not suited to distinguish between old divergences with gene flow and cases of recent divergence with isolation []. To address this problem and further investigate the timing of population splits and gene flow, we therefore employed different complementary modeling and phylogenetic approaches.

31 Beaumont M.A.

Zhang W.

Balding D.J. Approximate Bayesian computation in population genetics. 32 Meijaard, E. (2004). Solving mammalian riddles: a reconstruction of the Tertiary and Quaternary distribution of mammals and their palaeoenvironments in island South-East Asia. PhD thesis (Australian National University). Figure 3 Demographic History and Gene Flow in Pongo Show full caption (A) Model selection by ABC of plausible colonization histories of orangutans on Sundaland. The ABC analyses are based on the comparison of ∼3,000 non-coding 2-kb loci randomly distributed across the genome with corresponding data simulated under the different demographic models. The numbers in the black boxes indicate the model’s posterior probability. NT, Sumatran populations north of Lake Toba; ST, the Sumatran population of Batang Toru south of Lake Toba; BO, Bornean populations. e ). Arrows indicate gene flow among populations, and numbers above the arrows represent point estimates of numbers of migrants per generation. See also (B) ABC parameter estimates based on the full demographic model with colonization pattern inferred in (A). Numbers in gray rectangles represent point estimates of effective population size (N). Arrows indicate gene flow among populations, and numbers above the arrows represent point estimates of numbers of migrants per generation. See also Table S5 −8 per site per generation. See also (C) Relative cross-coalescent rate (RCCR) analysis for between-species pairs of phased high-coverage genomes. A RCCR close to 1 indicates extensive gene flow between species, and a ratio close to 0 indicates genetic isolation between species pairs. The x axis shows time scaled in years, assuming a generation time of 25 years and an autosomal mutation rate of 1.5 × 10per site per generation. See also Figure S3 We applied an approximate Bayesian computation (ABC) approach, which allows inference and comparison of arbitrarily complex demographic modes based on the comparison of the observed genomic data to extensive population genetic simulations []. Our analyses revealed three deep evolutionary lineages in extant orangutans ( Figures 3 A and 3B ). Colonization scenarios in which the earliest split within Pongo occurred between the lineages leading to P. abelii and P. tapanuliensis were much better supported than scenarios in which the earliest split was between Bornean and Sumatran species (model 1 versus model 2, combined posterior probability: 99.91%; Figure 3 A). Of the two best scenarios, a model postulating colonization of both northern Sumatra and Borneo from an ancestral population most likely situated south of Lake Toba on Sumatra had the highest support (model 1a versus model 1b, posterior probability: 97.56%; Figure 3 A). Our results supported a scenario in which orangutans from mainland Asia first entered Sundaland south of what is now Lake Toba on Sumatra, the most likely entry point based on paleogeographic reconstructions []. This ancestral population, of which P. tapanuliensis is a direct descendant, then served as a source for the subsequent different colonization events of what is now Borneo, Java, and northern Sumatra.

We estimated the split time between populations north and south of Lake Toba at ∼3.4 Ma ( Figure 3 B; Table S5 ). Under our best-fitting model, we found evidence for post-split gene flow across Lake Toba (∼0.3–0.9 migrants per generation; Table S5 ), which is consistent with highly significant signatures of gene flow between P. abelii and P. tapanuliensis using D statistics (CK, BT, WA, Homo sapiens: D = −0.2819, p < 0.00001; WK, BT, LK, Homo sapiens: D = −0.2967, p < 0.00001). Such gene flow resulted in higher autosomal affinity of P. tapanuliensis to P. abelii compared to P. pygmaeus in the PCA ( Figure 2 B), explaining the smaller amount of variance captured by PC2 (separating P. tapanuliensis from all other populations) compared to PC1 (separating P. pygmaeus from the Sumatran populations). The parameter estimates from a Bayesian full-likelihood analysis implemented in the software G-PhoCS were in good agreement with those obtained by the ABC analysis, although the split time between populations north and south of Lake Toba was more recent (∼2.27 Ma; 95% highest posterior density [HPD]: 2.21–2.35; Table S5 ). The G-PhoCS analysis revealed highly asymmetric gene flow between populations north and south of the Toba caldera, with much lower levels of gene flow into the Batang Toru population from the north than vice versa ( Table S5 ).

Figure 4 Sex-Specific Evolutionary History of Orangutans Show full caption Bayesian phylogenetic trees for (A) mitochondrial genomes and (B) Y chromosomes. The mitochondrial tree is rooted with a human and a central chimpanzee sequence and the Y chromosome tree with a human sequence (not shown). ∗∗Posterior probability = 1.00. (C) Genotype-sharing matrix for mitogenomes (above the diagonal) and Y chromosomes (below the diagonal) for all analyzed male orangutans. A value of 1 indicates that two males have identical genotypes at all polymorphic sites; a value of 0 means that they have different genotypes at all variable positions. The existence of two deep evolutionary lineages among extant Sumatran orangutans was corroborated by phylogenetic analyses based on whole mitochondrial genomes ( Figure 4 A), in which the deepest split occurred between populations north of Lake Toba and all other orangutans at ∼3.97 Ma (95% HPD: 2.35–5.57). Sumatran orangutans formed a paraphyletic group, with P. tapanuliensis being more closely related to the Bornean lineage from which it diverged ∼2.41 Ma (1.26–3.42 Ma). In contrast, Bornean populations formed a monophyletic group with a very recent mitochondrial coalescence at ∼160 ka (94–227 ka).

33 Arora N.

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et al. Parentage-based pedigree reconstruction reveals female matrilineal clusters and male-biased dispersal in nongregarious Asian great apes, the Bornean orang-utans (Pongo pygmaeus). 34 Nater A.

Nietlisbach P.

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et al. Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant Orangutans (genus: Pongo). Due to strong female philopatry [], gene flow in orangutans is almost exclusively male mediated []. Consistent with these pronounced differences in dispersal behavior, phylogenetic analysis of extensive Y chromosome sequencing data revealed a comparatively recent coalescence of Y chromosomes of all extant orangutans ∼430 kya ( Figure 4 B). The single available Y-haplotype from P. tapanuliensis was nested within the other Sumatran sequences, pointing at the occurrence of male-mediated gene flow across the Toba divide. Thus, in combination with our modeling results, the sex-specific data highlighted the impact of extraordinarily strong male-biased dispersal in the speciation process of orangutans.

35 Chesner C.A.

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Westgate J.A. Eruptive history of earths largest Quaternary caldera (Toba, Indonesia) clarified. 7 Wich S.A.

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et al. Land-cover changes predict steep declines for the Sumatran orangutan (Pongo abelii). Our analyses revealed significant divergence between P. tapanuliensis and P. abelii ( Figures 3 B and 4 A) and low levels of male-mediated gene flow ( Figures 3 B and 4 B), which, however, completely ceased 10–20 kya ( Figure 3 C). Populations north and south of Lake Toba on Sumatra had been in genetic contact for most of the time since their split, but there was a marked reduction in gene flow after ∼100 ka ( Figure 3 C), consistent with habitat destruction caused by the Toba supereruption 73 kya []. However, P. tapanuliensis and P. abelii have been on independent evolutionary trajectories at least since the late Pleistocene/early Holocene, as gene flow between these populations has ceased completely 10–20 kya ( Figure 3 C) and is now impossible because of habitat loss in areas between the species’ ranges [].

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et al. Ancient gene flow from early modern humans into Eastern Neanderthals. Nowadays, most biologists would probably adopt an operational species definition such as “a species is a population (or group of populations) with fixed heritable differences from other such populations (or groups of populations)” []. With totally allopatric populations, a “reproductive isolation” criterion, such as is still espoused by adherents of the biological species concept, is not possible []. Notwithstanding a long-running debate about the role of gene flow during speciation and genetic interpretations of the species concept [], genomic studies have found evidence for many instances of recent or ongoing gene flow between taxa that are recognized as distinct and well-established species. This includes examples within each of the other three hominid genera. A recent genomic study using comparable methods to ours revealed extensive gene flow between Gorilla gorilla and G. beringei until ∼20–30 ka []. Similar, albeit older and less extensive, admixture occurred between Pan troglodytes and P. paniscus [] and was also reported for Homo sapiens and H. neanderthalensis []. Pongo tapanuliensis and P. abelii appear to be further examples, showing diagnostic phenotypic and other distinctions that had persisted in the past despite gene flow between them.

44 Alba D.M.

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et al. New Oligocene primate from Saudi Arabia and the divergence of apes and Old World monkeys. Due to the challenges involved in collecting suitable specimens for morphological and genomic analyses from critically endangered great apes, our description of P. tapanuliensis had to rely on a single skeleton and two individual genomes for our main lines of evidence. When further data become available, a more detailed picture of the morphological and genomic diversity within this species and of the differences to other Pongo species might emerge, which may require further taxonomic revision. However, is not uncommon to describe species based on a single specimen (e.g., []), and, importantly, there were consistent differences among orangutan populations from multiple independent lines of evidence, warranting the designation of a new species with the limited data at hand.

7 Wich S.A.

Singleton I.

Nowak M.G.

Utami Atmoko S.S.

Nisam G.

Arif S.M.

Putra R.H.

Ardi R.

Fredriksson G.

Usher G.

et al. Land-cover changes predict steep declines for the Sumatran orangutan (Pongo abelii). 47 IUCN (2016). IUCN Red List of Threatened Species, version 2016.2. http://www.iucnredlist.org/. 48 Hedrick P.W.

Kalinowski S.T. Inbreeding depression in conservation biology. 49 Allendorf F.W.

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Aitken S.N. Conservation and the Genetics of Populations. With a census size of fewer than 800 individuals [], P. tapanuliensis is the least numerous of all great ape species []. Its range is located around 100 km from the closest population of P. abelii to the north ( Figure 2 A). A combination of small population size and geographic isolation is of particularly high conservation concern, as it may lead to inbreeding depression [] and threaten population persistence []. Highlighting this, we discovered extensive runs of homozygosity in the genomes of both P. tapanuliensis individuals ( Figure S3 ), pointing at the occurrence of recent inbreeding.