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The Genetic Basis for Adaptation in Natural Populations

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The Genetic Basis for Adaptation in Natural Populations Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 1192 The genetic basis for adaptation in natural populations SANGEET LAMICHHANEY ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6206 ISBN 978-91-554-9502-2 UPPSALA urn:nbn:se:uu:diva-279969 2016 Dissertation presented at Uppsala University to be publicly examined in B41, BMC, Husargätan 3, Uppsala, Friday, 29 April 2016 at 13:15 for the degree of Doctor of Philosophy (Faculty of Medicine). The examination will be conducted in English. Faculty examiner: Professor Henrik Kaessmann (Heidelberg University, Germany). Abstract Lamichhaney, S. 2016. The genetic basis for adaptation in natural populations. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine 1192. 60 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-554-9502-2. Many previous studies in evolutionary genetics have been based on few model organisms that can be reared at ease in the laboratory. In contrast, genetic studies of non-model, natural populations are desirable as they provide a wider range of adaptive phenotypes throughout evolutionary timescales and allow a more realistic understanding of how natural selection drives adaptive evolution. This thesis represents an example of how modern genomic tools can be effectively used to study adaptation in natural populations. Atlantic herring is one of the world’s most numerous fish having multiple populations with phenotypic differences adapted to strikingly different environments. Our study demonstrated insignificant level of genetic drift in herring that resulted in minute genetic differences in the majority of the genome among these populations. In contrast, a small percentage of the loci showed striking genetic differentiation that were potentially under natural selection. We identified loci associated with adaptation to the Baltic Sea and with seasonal reproduction (spring- and autumn-spawning) and demonstrated that ecological adaptation in Atlantic herring is highly polygenic but controlled by a finite number of loci. The study of Darwin’s finches constitutes a breakthrough in characterizing their evolution. We identified two loci, ALX1 and HMGA2, which most likely are the two most prominent loci that contributed to beak diversification and thereby to expanded food utilization. These loci have played a key role in adaptive evolution of Darwin’s finches. Our study also demonstrated that interspecies gene flow played a significant role in the radiation of Darwin’s finches and some species have a mixed ancestry. This thesis also explored the genetic basis for the remarkable phenotypic differences between three male morphs in the ruff. Identification of two different versions of a 4.5 MB inversion in Satellites and Faeders that occurred about 4 million years ago revealed clues about the genetic foundation of male mating strategies in ruff. We highlighted two genes in the inverted region; HSD17B2 that affects metabolism of testosterone and MC1R that has a key role in regulating pigmentation, as the major loci associated with this adaptation. Keywords: Adaptive evolution, Atlantic herring, ecological adaptation, seasonal reproduction, TSHR, Darwin’s finches, natural selection, beak, ALX1, HMGA2, ruff, lek, inversion, HSD17B2, MC1R Sangeet Lamichhaney, Department of Medical Biochemistry and Microbiology, Box 582, Uppsala University, SE-75123 Uppsala, Sweden. © Sangeet Lamichhaney 2016 ISSN 1651-6206 ISBN 978-91-554-9502-2 urn:nbn:se:uu:diva-279969 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-279969) The measure of intelligence is the ability to change - Albert Einstein Cover images: (1) Herring in the Baltic Sea © Riku Lumiaro/Finnish Envi- ronment Institute (2) Medium ground finch © P. R. Grant, originally pub- lished in Grant & Grant (2014) and (3) Independent male ruff dominating Satellite male at lek © Torsten Green-Petersen List of papers This thesis is based on the following five papers I. Sangeet Lamichhaney*, Alvaro Martinez Barrio*, Nima Rafati*, Görel Sundstrom*, Carl-Johan Rubin, Elizabeth R. Gilbert, Jonas Berglund, Anna Wetterbom, Linda Laikre, Matthew T. Webster, Manfred Grabherr, Nils Ryman and Leif Andersson (2012) Population-scale sequencing reveals genetic differ- entiation due to local adaptation in Atlantic herring. Proceedings of the Nation- al Academy of Sciences U.S.A. 109, 19345-19350. II. Alvaro Martinez Barrio*, Sangeet Lamichhaney*, Guangyi Fan*, Nima Ra- fati*, Mats Pettersson, He Zhang, Jacques Dainat, Diana Ekman, Marc Hoeppner, Patric Jern, Marcel Martin, Björn Nystedt, Xin Liu, Wenbin Chen, Xinming Liang, Chengcheng Shi, Yuanyuan Fu, Kailong Ma, Xiao Zhan, Chungang Feng, Ulla Gustafson, Carl-Johan Rubin, Markus Sällman Almén, Martina Blass, Michele Casini, Arild Folkvord, Linda Laikre, Nils Ryman, Si- mon Ming-Yuen Lee, Xun Xu and Leif Andersson, The genetic basis for eco- logical adaptation of the Atlantic herring revealed by genome sequencing, Manuscript under review. III. Sangeet Lamichhaney*, Jonas Berglund*, Markus Sällman Almén, Khurram Maqbool, Manfred Grabherr, Alvaro Martinez-Barrio, Marta Promerova´, Carl- Johan Rubin, Chao Wang, Neda Zamani, B. Rosemary Grant, Peter R. Grant, Matthew T. Webster and Leif Andersson (2015) Evolution of Darwin's finches and their beaks revealed by genome sequencing. Nature 518, 371-375 IV. Sangeet Lamichhaney, Fan Han, Jonas Berglund, Chao Wang, Markus Säll- man Almén, Matthew T. Webster, B. Rosemary Grant, Peter R. Grant and Leif Andersson, A beak size locus in Darwin’s finches facilitated character dis- placement during a drought, Science, in press . V. Sangeet Lamichhaney*, Guangyi Fan*, Fredrik Widemo*, Ulrika Gunnars- son, Doreen Schwochow Thalmann, Marc P Hoeppner, Susanne Kerje, Ulla Gustafson, Chengcheng Shi, He Zhang, Wenbin Chen, Xinming Liang, Leihuan Huang, Jiahao Wang, Enjing Liang, Qiong Wu, Simon Ming-Yuen Lee, Xun Xu, Jacob Höglund, Xin Liu and Leif Andersson (2016) Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax), Nature Genetics, 48, 84-88. * These authors contributed equally Reprints were made with permission from the respective publishers. List of papers (not included in the thesis) I. Markus Sällman Almén, Sangeet Lamichhaney, Jonas Berglund, B. Rosemary Grant, Peter R. Grant, Matthew T. Webster and Leif Andersson (2015) Adaptive radiation of Darwin’s finches revisited using whole genome sequencing, Bioessays, 38, 14-20. II. Suzanne V. Saenko, Sangeet Lamichhaney, Alvaro Martinez Barrio, Nima Rafati, Leif Andersson and Michel C. Milinkovitch (2015) Amelanism in the corn snake is caused by the insertion of an LTR-retrotransposon in the OCA2 gene, Scientific Reports, 5, 17118. III. Mats E. Pettersson, Marcin Kierczak, Markus Sällman Almén, Sangeet Lamich- haney and Leif Andersson, A model-free approach for detecting genomic regions of deep divergence using the distribution of haplotype distances, Manuscript sub- mitted. IV. Neda Zamani*, Behrooz Torabi Moghadam*, Nima Rafati*, Sangeet Lamich- haney*, Görel Sundström, Henrik Lantz, Alvaro Martinez Barrio, Jan Komor- owski, Bernardo J. Clavijo, Patric Jern and Manfred G Grabherr, A local web inter- face for protein and transcript aligners: Smörgås, Manuscript submitted * These authors contributed equally Table of contents 1. Introduction ............................................................................................... 13 1.1. Adaptation ......................................................................................... 13 1.2. Genetics of adaptation ....................................................................... 14 1.3. The ‘Genomics’ of adaptation ........................................................... 15 1.4. Methods to identify loci underlying adaptation ................................. 15 1.4.1. Forward genetics approaches ..................................................... 15 1.4.2. Reverse genetics approaches ...................................................... 18 1.4.3. Candidate genes approaches ...................................................... 19 1.5. Background to the thesis projects ...................................................... 20 1.5.1. Atlantic herring .......................................................................... 20 1.5.2. Darwin’s finches ........................................................................ 22 1.5.3. Ruff ............................................................................................ 25 2. Methods ..................................................................................................... 28 2.1. Sampling and collection of ecological data ....................................... 28 2.2. Whole-genome sequencing ................................................................ 29 2.3. Variant discovery and downstream analysis ..................................... 29 2.4. Genome-wide screen for genetic differentiation ............................... 30 2.5. Underlying genetic basis for adaptive divergence ............................. 30 2.6. Further characterization of candidate loci ......................................... 31 3. Results and Discussion .............................................................................. 32 3.1. Herring ............................................................................................... 32 3.1.1. Paper I ........................................................................................ 32 3.1.2. Paper II ......................................................................................
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