Marked Population Structure and Recent Migration in the Critically Endangered Sumatran Orangutan (Pongo abelii)

Abstract

A multitude of factors influence how natural populations are genetically structured, including dispersal barriers, inhomogeneous habitats, and social organization. Such population subdivision is of special concern in endangered species, as it may lead to reduced adaptive potential and inbreeding in local subpopulations, thus increasing the risk of future extinctions. With only 6600 animals left in the wild, Sumatran orangutans (Pongo abelii) are among the most endangered, but also most enigmatic, great ape species. In order to infer the fine-scale population structure and connectivity of Sumatran orangutans, we analyzed the most comprehensive set of samples to date, including mitochondrial hyper-variable region I haplotypes for 123 individuals and genotypes of 27 autosomal microsatellite markers for 109 individuals. For both mitochondrial and autosomal markers, we found a pronounced population structure, caused by major rivers, mountain ridges, and the Toba caldera. We found that genetic diversity and corresponding long-term effective population size estimates vary strongly among sampling regions for mitochondrial DNA, but show remarkable similarity for autosomal markers, hinting at male-driven long-distance gene flow. In support of this, we identified several individuals that were most likely sired by males originating from other genetic clusters. Our results highlight the effect of natural barriers in shaping the genetic structure of great ape populations, but also point toward important dispersal corridors on northern Sumatra that allow for genetic exchange.

Effective Characterisation of the Complete Orang-Utan Mitochondrial DNA Control Region, in the Face of Persistent Focus in Many Taxa on Shorter Hypervariable Regions

“…To demonstrate the forensic utility of progressively longer sequences, we cut our alignment to the various lengths of those published and analysed in six prior studies: 244 positions [41]; 325 positions [45,46]; 387 positions [48]; 409 positions [47] and 422 positions [49] (for nucleotide positions, see Table 1). In the case of the latter two studies, for which the authors chose not to release their sequences, we cut the alignment based on the length of the analysed sequences specified in each manuscript.…”

“…For each, we either: 1) re-aligned the sequences with those derived from Bornean orang-utans of known geographic origin [45], and cut the alignment to the length of the predominantly analysed 323 bp segment; or 2) excised the 323 bp segment predominantly analysed for Bornean orang-utans, concatenated the remaining bases, and re-aligned the nucleotides. We repeated this procedure for Sumatran orang-utans, with published sequences from individuals of known origin on Sumatra [48], instead cutting the alignment to the 385 bp segment predominantly analysed in this species. We inferred phylogenetic trees from all alignments, and from an alignment of only all complete control-region sequences, with which to compare the consistency of inferred evolutionary relationships.…”

“…The remainder of all published control-region sequences were all considerably shorter in length, and all comprise only the left domain or parts thereof. Two segments within this domain are predominant: among Sumatran orang-utans, a ~385 bp segment [48]; among Bornean orang-utans, a ~323 bp segment [45,46] encompassed within the former.…”

Genetic and genomic monitoring with minimally invasive sampling methods

“…For many species, genetic-diversity based estimates that provide long-term effective population sizes can be the only way to infer historical abundance (e.g., Beerli & Felsenstein, 2001). While this approach has its limitations and caveats (Palsbøll et al, 2013), MIS have been used to estimate long-term effective population sizes in species such as southern right whales (Carroll et al, 2015) and Sumatran orangutans (Pongo abelii; Nater et al, 2013). Historical samples can provide a direct way of assessing past levels of genetic diversity and effective population size, and therefore any recent changes in these metrics.…”

Great ape Y Chromosome and mitochondrial DNA phylogenies reflect subspecies structure and patterns of mating and dispersal

“…Autosomal analysis has typically focused on analysis of short tandem repeats (STRs) (e.g., Becquet et al 2007;Nater et al 2013;Fünfstück et al 2014), with increasing numbers of whole-genome sequences recently becoming available (Prado-Martinez et al 2013;Xue et al 2015) and providing a rich picture of population structure and demographic history. Maternally inherited mitochondrial DNA (mtDNA) has also been widely exploited, progressing from sequencing of the hypervariable regions (Fischer et al 2006) to the maximum possible resolution of the whole molecule (Hvilsom et al 2014).…”