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Comparative Study
, 469 (7331), 529-33

Comparative and Demographic Analysis of Orang-Utan Genomes

Devin P Locke  1 LaDeana W HillierWesley C WarrenKim C WorleyLynne V NazarethDonna M MuznyShiaw-Pyng YangZhengyuan WangAsif T ChinwallaPat MinxMakedonka MitrevaLisa CookKim D DelehauntyCatrina FronickHeather SchmidtLucinda A FultonRobert S FultonJoanne O NelsonVincent MagriniCraig PohlTina A GravesChris MarkovicAndy CreeHuyen H DinhJennifer HumeChristie L KovarGerald R FowlerGerton LunterStephen MeaderAndreas HegerChris P PontingTomas Marques-BonetCan AlkanLin ChenZe ChengJeffrey M KiddEvan E EichlerSimon WhiteStephen SearleAlbert J VilellaYuan ChenPaul FlicekJian MaBrian RaneyBernard SuhRichard BurhansJavier HerreroDavid HausslerRui FariaOlga FernandoFleur DarréDomènec FarréElodie GazaveMeritxell OlivaArcadi NavarroRoberta RobertoOronzo CapozziNicoletta ArchidiaconoGiuliano Della ValleStefania PurgatoMariano RocchiMiriam K KonkelJerilyn A WalkerBrygg UllmerMark A BatzerArian F A SmitRobert HubleyClaudio CasolaDaniel R SchriderMatthew W HahnVictor QuesadaXose S PuenteGonzalo R OrdoñezCarlos López-OtínTomas VinarBrona BrejovaAakrosh RatanRobert S HarrisWebb MillerCarolin KosiolHeather A LawsonVikas TaliwalAndré L MartinsAdam SiepelArindam RoychoudhuryXin MaJeremiah DegenhardtCarlos D BustamanteRyan N GutenkunstThomas MailundJulien Y DutheilAsger HobolthMikkel H SchierupOliver A RyderYuko YoshinagaPieter J de JongGeorge M WeinstockJeffrey RogersElaine R MardisRichard A GibbsRichard K Wilson
Affiliations
Comparative Study

Comparative and Demographic Analysis of Orang-Utan Genomes

Devin P Locke et al. Nature.

Abstract

'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.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1. Divergence among great apes, a lesser ape, and an old world monkey with respect to humans
We estimated nucleotide divergence in unique gap-free sequence, indicated at each node, from the alignment of rhesus macaque (yellow), gibbon (purple), orangutan (orange), gorilla (aqua), chimpanzee (green) and human (blue) whole genome shotgun reads to the human reference (Hs.35)(S3). Note that the Bornean (Pongo pygmaeus) and Sumatran (Pongo abelii) orangutan species showed nucleotide identity comparable to that of bonobo (Pan paniscus) and chimpanzee (Pan troglodytes). *Yu et al. 2003, #Chen and Li 2001.
Figure 2
Figure 2. The neocentromere of orangutan chromosome 12
Note the identical order of four BAC-derived FISH probes (IDs in S8) between the normal (left panel) and neocentromere-bearing (right panel) configurations of orangutan chromosome 12, despite discordant centromere positions indicated by arrows on the adjacent DAPI-only images. The neocentromere recruits centromeric proteins CENP-A and CENP-C and lies within a ~225 kb gene-free and alpha satellite-free region. The neocentromere-bearing variant is polymorphic in both Bornean and Sumatran populations, suggesting the neocentromere arose prior to the Bornean/Sumatran split, yet has not been fixed in either species.
Figure 3
Figure 3. Alu quiescence in the orangutan lineage
We identified only ~250 lineage-specific Alu retroposition events in the orangutan genome, a dramatically lower rate than that of other sequenced primates, including humans. The total number of lineage-specific L1, SVA and Alu insertions is shown (pie chart), along with the rate of insertion events per element type (bar graph). Reduced Alu retroposition potentially limited the effect of a wide variety of repeat-driven mutational mechanisms in the orangutan lineage that played a major role in restructuring other primate genomes.
Figure 4
Figure 4. Enrichment for positive selection in the cerebroside-sulfatid metabolism pathway
We identified six genes (indicated in yellow) under moderate to strong positive selection in primates (P<0.05) that fall within the cerebroside-sulfatid region of the sphingolipid metabolism pathway (adapted from human KEGG pathway 00600; http://www.genome.jp/kegg/kegg2.html). This pathway is associated with several human lysosomal storage disorders, such as Gaucher’s disease, Sandhoff’s disease, Tay Sachs disease and metachromatic leukodystrophy.
Figure 5
Figure 5. Orangutan population genetics and demographics
a. Site-frequency spectra (SFS) for 13.2 million Bornean (blue) and Sumatran (red) SNPs are shown, note the enrichment of low-frequency SNPs among Sumatran individuals. b. The majority of SNPs were restricted to their respective island populations as the ‘heat’ of the 2D SFS, representing high allele counts, lay along the axes. c. Our demographic model estimated the ancestral orangutan population (Ne = 17,900) split approximately 400,000 years ago, followed by exponential expansion of Sumatran Ne and a decline of Bornean Ne, culminating in higher diversity among modern Sumatran orangutans despite a lower census population size. The model also supported low-level gene flow (<1 individual/generation) indicated by arrows.

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