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Unraveling the Evolutionary History of Orangutans (Genus: Pongo)- the Impact of Environmental Processes and the Genomic Basis of Adaptation

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Unraveling the Evolutionary History of Orangutans (Genus: Pongo)- the Impact of Environmental Processes and the Genomic Basis of Adaptation Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2015 Unraveling the evolutionary history of Orangutans (genus: Pongo)- the impact of environmental processes and the genomic basis of adaptation Mattle-Greminger, Maja Patricia Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-121397 Dissertation Published Version Originally published at: Mattle-Greminger, Maja Patricia. Unraveling the evolutionary history of Orangutans (genus: Pongo)- the impact of environmental processes and the genomic basis of adaptation. 2015, University of Zurich, Faculty of Science. Unraveling the Evolutionary History of Orangutans (genus: Pongo) — The Impact of Environmental Processes and the Genomic Basis of Adaptation Dissertation zur Erlangung der naturwissenschaftlichen Doktorwürde (Dr. sc. nat.) vorgelegt der Mathematisch‐naturwissenschaftlichen Fakultät der Universität Zürich von Maja Patricia Mattle‐Greminger von Richterswil (ZH) Promotionskomitee Prof. Dr. Carel van Schaik (Vorsitz) PD Dr. Michael Krützen (Leitung der Dissertation) Dr. Maria Anisimova Zürich, 2015 To my family Table of Contents Table of Contents ........................................................................................................ 1 Summary ..................................................................................................................... 3 Zusammenfassung ...................................................................................................... 7 Acknowledgments ................................................................................................... 11 1 General introduction .......................................................................................... 15 1.1 Evolutionary processes shaping patterns of genetic diversity ............................ 16 1.2 Processes shaping patterns of genetic variation in orangutans .......................... 16 1.3 The genomics revolution ..................................................................................... 26 1.4 Aims and outline of the dissertation ................................................................... 27 2 The quest for Y‐chromosomal markers – methodological strategies for mammalian non‐model organisms .................................................................... 33 2.1 Abstract ................................................................................................................ 34 2.2 Introduction ......................................................................................................... 35 2.3 Current methodological strategies ...................................................................... 38 2.4 Emerging methods ............................................................................................... 49 2.5 Conclusions .......................................................................................................... 51 3 Generation of SNP datasets for orangutan population genomics using improved reduced‐representation sequencing and direct comparisons of SNP calling algorithms ................................................................................................ 53 3.1 Abstract ................................................................................................................ 54 3.2 Introduction ......................................................................................................... 55 3.3 Results .................................................................................................................. 58 3.4 Discussion ............................................................................................................ 69 3.5 Methods ............................................................................................................... 73 3.6 Supporting Information ....................................................................................... 79 4 Orangutan demographic history and population structure inferred by genus‐ wide whole‐genome sequencing ....................................................................... 93 4.1 Abstract ................................................................................................................ 94 4.2 Introduction ......................................................................................................... 95 1 4.3 Materials and Methods ........................................................................................ 98 4.4 Results ................................................................................................................ 104 4.5 Discussion .......................................................................................................... 109 4.6 Supporting Information ..................................................................................... 113 5 Discordant sex‐specific evolutionary histories of orangutans inferred from deep sequencing of Y chromosomes and mitochondrial genomes ................ 123 5.1 Abstract .............................................................................................................. 124 5.2 Introduction ....................................................................................................... 125 5.3 Results ................................................................................................................ 128 5.4 Discussion .......................................................................................................... 136 5.5 Materials and Methods ...................................................................................... 139 5.6 Supporting Information ..................................................................................... 146 6 Whole‐genome scans detect potential genetic footprints of local adaptation in orangutans (genus Pongo) ............................................................................ 157 6.1 Abstract .............................................................................................................. 158 6.2 Introduction ....................................................................................................... 159 6.3 Materials and Methods ...................................................................................... 162 6.4 Results ................................................................................................................ 166 6.5 Discussion .......................................................................................................... 182 6.6 Supporting Information ..................................................................................... 187 7 General discussion and perspectives ............................................................... 207 7.1 The evolutionary history of the genus Pongo .................................................... 208 7.2 Implications for conservation and taxonomy .................................................... 213 7.3 Outlook .............................................................................................................. 215 List of additional publications ............................................................................... 219 References.............................................................................................................. 221 Reprints of some relevant co‐authored publications .......................................... 245 2 Summary Understanding how adaptive variation in phenotypic traits evolved by natural selection and contributed to the process of speciation is one of the central goals of evolutionary biology. Until recently, however, identifying the genetic basis and mechanisms underlying adaptation at the genome‐wide scale was technologically beyond reach. The advent of high‐throughput sequencing has transformed our ability to address basic questions of evolutionary genetics such as the relative importance of the processes shaping patterns of genetic variation within and among species. Orangutans (genus: Pongo) are the only Asian great apes and currently endemic to the Sundaland islands of Borneo (P. pygmaeus) and Sumatra (P. abelii). The Southeast Asian Sunda archipelago is a tropical hotspot of biodiversity with unusually high level of species endemism, making it to one of the most exciting global regions in which to investigate how environmental processes lead to local adaptation and species diversification. The region has been drastically affected by geological and environmental processes such as tectonic plate movements, Quaternary climatic oscillations, fluctuating sea levels, and volcanic eruptions. The Sunda Shelf was for instance cyclically exposed during glacial periods when sea levels were lower, which repeatedly reconnected the islands. Orangutans show remarkable, well‐documented geographic variation in various traits related to morphology, physiology, life history, behavioral ecology, and social organization, suggesting high levels of local adaptions. A considerable part of this variation is almost certainly linked to environmental differences throughout the genus’ range. The variation in phenotypic traits offers a great opportunity to investigate the interaction between environmental forces and genetic variation both between and within species. In this dissertation, I studied the evolutionary history of the genus Pongo, i.e. how environmental processes in Sundaland shaped
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