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Speciation Genetics of Recently Diverged Species Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1714 Speciation genetics of recently diverged species VENKAT TALLA ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0429-8 UPPSALA urn:nbn:se:uu:diva-358292 2018 Dissertation presented at Uppsala University to be publicly examined in Lindahlsalen, Evolutionary Biology Centre, Norbyvagan 18, Uppsala, Friday, 19 October 2018 at 10:15 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Dr Nicola Nadeau (University of Sheffield). Abstract Talla, V. 2018. Speciation genetics of recently diverged species. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1714. 74 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0429-8. Species differentiation can be a consequence of evolutionary forces including natural selection and random genetic drift. Patterns of genomic differentiation vary across the tree of life. This variation seems to be dependent on, for example, differences in genomic architecture and molecular mechanisms. However, the knowledge we currently possess, both regarding the processes driving speciation and the resulting genomic signatures, is from a very small subset of the overall biodiversity that resides on the planet. Therefore, characterization of the architecture of genomic divergence from more organism groups will be important to understand the effects of molecular mechanisms and evolutionary forces driving divergence between lineages. Hence it has not been possible to come to a consensus on the relative importance of genetic drift and natural selection on divergence processes in general. In this thesis, I use genomic approaches to investigate the forces underlying species and population differentiation in the European cryptic wood white butterflies (Leptidea sinapis, L. reali and L. juvernica) and two closely related bird species, the chiffchaff (Phylloscopus collybita abietinus) and the Siberian chiffchaff (P. tristis). Both these groups contain recently diverged species, a prerequisite for investigating initial differentiation processes. However, the study systems also differ in several respects, allowing for applying distinct approaches to understand the divergence process in each system. In summary, by applying a suite of genomic approaches, my thesis work gives novel insights into the speciation history of wood whites and chiffchaff. I identify candidate genes for local adaptation in both systems and concludes that genome differentiation in wood white butterflies have been driven by a combination of random genetic drift and week directional selection in allopatry. In the chiffchaff, the general differentiation landscape seems to have been shaped by recurrent background selection (and potentially selective sweeps), likely as a consequence of regional variation in the recombination rate which has also been observed in other genome- scans in birds. Potentially, some of the highly differentiated regions contain barriers to gene- flow as these regions are still present in sympatry, where species exchange genetic material at a high rate. Keywords: Speciation, Leptidea, Lepidoptera, chiffchaff, Cryptic species, genome-scan, Diapause Venkat Talla, Department of Ecology and Genetics, Evolutionary Biology, Norbyvägen 18D, Uppsala University, SE-75236 Uppsala, Sweden. © Venkat Talla 2018 ISSN 1651-6214 ISBN 978-91-513-0429-8 urn:nbn:se:uu:diva-358292 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-358292) To Mom & Dad List of Papers I Talla, V., Suh, A., Kalsoom, F., Dincă, V., Vila, R., Friberg, M., Wiklund, C. and Backström, N. (2017) Rapid increase in genome size as a consequence of transposable element hyperactivity in wood-white (Leptidea) butterflies. Genome Biology and Evolu- tion, 9(10), 2491-2505. II Talla, V., Johansson, A., Dincă, V., Vila, R., Friberg, M., Wiklund, C. and Backström, N. Lack of parallelism: lineage-spe- cific directional selection drives genome differentiation across a triplet of cryptic butterfly species. Submitted manuscript. III Talla, V., Kalsoom, F., Shipilina, D., Marova, I. and Backström, N. (2017) Heterogeneous Patterns of Genetic Diversity and Dif- ferentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis). G3: Genes, Genomes, Genetics, 7(12), 3983-3998. IV Talla, V., Soler, L., Kawakami, T.,, Dincă, V., Vila, R., Friberg, M., Wiklund, C. and Backström, N. Dissecting the effects of na- tural selection and mutation on genetic diversity in three recently diverged cryptic butterfly species. Manuscript. V Leal, L.*, Talla, V.*, Källman, T., Friberg, M., Wiklund, C., Dincă, V., Vila, R. and Backström, N. (2018) Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation. Molecular Ecology, 27(4), 935-948. * These authors contributed equally to the study. Reprints were made with permission from the respective publishers. Contents 1. Introduction ............................................................................................... 11 1.1 Speciation ........................................................................................... 13 1.2 Speciation genes ................................................................................. 15 1.3 Local adaptation ................................................................................. 16 1.3.1 Identifying genes responsible for divergent traits ....................... 17 1.3.2 Effect of hybridization ................................................................ 18 1.3.3 Effect of genetic drift .................................................................. 20 1.4 Genome evolution .............................................................................. 21 1.4.1 Evolution of transposable elements ............................................ 21 1.4.2 Evolution of protein coding genes .............................................. 22 1.5 Gene expression differences ............................................................... 23 1.6 Cryptic species ................................................................................... 24 1.7 Diapause ............................................................................................. 25 2. Methods .................................................................................................... 26 2.1 Study systems ..................................................................................... 26 2.1.1 The wood white butterflies ......................................................... 26 2.1.2 The common chiffchaff .............................................................. 28 2.2 Genome sequencing and assembly ..................................................... 29 2.3 Population re-sequencing ................................................................... 31 2.4 Population genetics ............................................................................ 32 2.4.1 Inference of demographic history ............................................... 32 2.4.2 Detecting population structure .................................................... 33 2.4.3 Introgression analysis ................................................................. 33 2.4.4 Genome wide patterns of diversity and differentiation ............... 34 2.4.5 Selection tests ............................................................................. 35 2.5 Gene annotation .................................................................................. 36 2.6 RNA sequencing and gene expression ............................................... 36 3. Research aims ........................................................................................... 38 3.1 General aims ....................................................................................... 38 3.2 Scientific aims .................................................................................... 39 4. Paper summaries ....................................................................................... 41 5. Conclusions and future projects ................................................................ 48 Svensk sammanfattning ................................................................................ 51 Acknowledgements ....................................................................................... 53 References ..................................................................................................... 55 Abbreviations DNA Deoxyribonucleic acid RNA Ribonucleic acid SNP Single nucleotide polymorphism Indel Insertion and deletion 4D sites 4 fold degenerate sites TE Transposable element TMRCA Time to the most recent common ancestor Mb Mega base pairs Kb Kilo base pairs bp Base pair My Million years 10 1. Introduction The vast diversity of species that resides on earth has probably always been fascinating to mankind. Naming and clustering of organisms into groups has been done by civilisations since the beginning of written language (Stevens, 2001). Although several civilisations classified organisms in their own lan- guages, the most known early classifications were conducted by early Greek philosophers Aristotle and his student Theophrastus (Stevens, 2001). It wasn’t until 1758 that a Swedish scientist named Carl Linnaeus classified organisms using binomial nomenclature and by clustering similar organisms into groups called taxa (Linnaeus,
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