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. 2013 Oct 23;8(10):e77175.
doi: 10.1371/journal.pone.0077175. eCollection 2013.

Population genomic analysis reveals a rich speciation and demographic history of orang-utans (Pongo pygmaeus and Pongo abelii)

Xin Ma  1 , Joanna L Kelley, Kirsten Eilertson, Shaila Musharoff, Jeremiah D Degenhardt, André L Martins, Tomas Vinar, Carolin Kosiol, Adam Siepel, Ryan N Gutenkunst, Carlos D Bustamante
Affiliations

Population genomic analysis reveals a rich speciation and demographic history of orang-utans (Pongo pygmaeus and Pongo abelii)

Xin Ma et al. PLoS One. .

Abstract

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.

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Conflict of interest statement

Competing Interests: CDB is on the Scientific or Medical Advsiory Board of several companies including Personalis, Inc., InVitae, and Ancestry.com. There are no patents, products in development or marketed products to declare. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

Figures

Figure 1
Figure 1. Phylogenetic tree of mtDNA HVRI region and allele sharing matrix of mtDNA and autosomes.
(A) The phylogenetic tree among human, chimpanzee, Bornean (red) and Sumatran (blue). The nodes shaded in cyan represent the grouping of the three Sumatran individuals that has the furthest distance to the rest clustering of the Sumatran group. The 10 re-sequenced individuals from our study are colored as red (Bornean) or blue (Sumatran). The corresponding geographic origins are shown on the right with the following annotation (SU: Sumatran; TU/SL: Tuanan or Sungai Lading; DV/K: Danum Valley or Kinabatangan; SA/GP: Sabangau or Gunung Palung; EK: East Kalimantan including Kutai national park or Sangatta; SAR/DS: Semongok Wildlife Rehabilitation Centre or Danau Sentarum). (B) The IBS allele sharing matrix among the 10 individuals from our study with the same group coloring scheme. The upper and lower triangular matrix represents the IBS sharing of all mtDNA variation loci (n = 1084) and autosomal variation loci (n = 11,866,619), respectively.
Figure 2
Figure 2. SFS analysis.
(A) SFS for all genomic SNPs (Genome), synonymous (S) or non-synonymous (NS) SNPs in Bornean (Red) and Sumatran (Blue) population. (B) Two-dimensional SFS (Bornean on Y axis and Sumatran on X axis). Top row: Spectra for different functional categories of SNPs. To make all the spectra directly comparable, the non-coding and synonymous spectra have been re-scaled to represent the same number of segregating SNPs as the non-synonymous spectrum. Bottom row: residuals between pairs of spectra. Bottom-left compares synonymous and non-coding spectra, and bottom-right compares non-synonymous and synonymous spectra. Red and blue entries indicate, respectively, that the first spectrum has greater or fewer SNPs in that entry than the second.
Figure 3
Figure 3. Distribution of the proportion SNPs within each of the PolyPhen categories based on PolyPhen-2 result.
Error bars denote 95% confidence intervals on the proportion of SNPs in each category.
Figure 4
Figure 4. Inferred cumulative distribution of selection coefficients.
Solid lines are for the full demographic model, dashed are for the model with no migration, and dotted are for the model with no growth. The break in the axes indicates that the scale is not continuous, because a logarithmic scale cannot span zero.
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