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Processes underlying genetic differentiation and speciation in orangutans (Pongo spp.)

Processes underlying genetic differentiation and speciation in orangutans (Pongo spp.)
Alexander Nater

2011

Institute of Evolutionary Biology and Environmental Studies, University of Zurich, 8006 Zürich, SWITZERLAND.

ABSTRACT

A fundamental topic in evolutionary biology deals with the processes that led to genetic structuring of populations. Such a subdivision of gene pools allows local populations to follow independent evolutionary trajectories, during which the influence of mutation, genetic drift and natural selection might finally lead to speciation. The specific role of environmental processes in shaping the distribution of genetic diversity within and between species is still a topic of debate. The Southeast Asian Sundaland region is of special interest to study the influence of environmental factors on patterns of genetic diversity. This region consists of three major and numerous smaller islands, which have been recurrently connected to form a single landmass during Pleistocene glacial periods. The insular dynamics have led to an extremely high biodiversity on Sundaland, with a large number of endemic species on different islands.

In this thesis, I studied the processes influencing genetic structuring, gene flow and diversification in orangutans (Pongo spp.), the only Asian great apes, and species that are closely related to humans. Fossil evidence indicates that these apes were once widespread in southeastern Asia, but are now restricted to rainforests of northern Sumatra (P. abelii) and Borneo (P. pygmaeus). Furthermore, the fragmentation of their habitat renders them highly susceptible to extinction. Despite the remarkable features of orangutans, their evolutionary history is still very poorly understood.

For this project, I used the most extensive set of genetic samples from wild orangutans available to date to investigate the role of climate and sea level changes during Pleistocene glaciations, volcanic activity, geographic barriers and sex-biased dispersal behavior in the evolutionary history of orangutans. Using a combination of different genetic marker systems, I found remarkable genetic patterns in both orangutan species. Female-transmitted mitochondrial lineages exhibited strong geographic structuring, which I attributed to a combination of pronounced female philopatry and geographic dispersal barriers, such as rivers and mountain ridges. Remarkably, the Toba volcano on northern Sumatra led to a strong and long-lasting separation of mitochondrial gene pools in orangutans, as the only remaining Sumatran population south of the Toba caldera is more closely related to Bornean orangutans than to their Sumatran conspecifics.

In contrast to the strong geographic structure of mitochondrial haplotypes, Y-chromosomal markers, which are male-transmitted, revealed little geographic structure within each species and point toward a strong male bias in gene flow among orangutan populations. Male orangutans were able to distribute genes over large distances, as evidenced by my finding that regular genetic exchange between Bornean and Sumatran orangutans occurred until the beginning of the last glacial period ~110 kya.

Furthermore, by employing a novel modeling approach, I was able to shed light on the demographic history of the two orangutan species and investigate the impact of climate changes and anthropogenic factors on population sizes and connectedness. This approach revealed a marked difference in the demographic history of both orangutan species. Bornean orangutans were strongly influenced by recurrent changes in rainforest coverage during Pleistocene glaciations, leading to at least one severe population bottleneck. In contrast, Sumatran orangutans displayed a remarkable stable demographic history until the end of the Pleistocene, when all Sumatran populations underwent a strong decline, most likely in response to increased hunting pressure by human colonizers.

In summary, I identified important environmental processes leading to genetic structuring and differentiation in orangutans. I showed that, under the influence of these environmental processes, orangutans experienced a complex demographic history, which led to distinct patterns of genetic variation. These findings will be of major importance for studies dealing with adaptive evolution in orangutans and other great apes.