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Functional Genomics of Diapause in Two Temperate Butterflies

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Functional Genomics of Diapause in Two Temperate Butterflies Functional genomics of diapause in two temperate butterflies Peter Pruisscher Academic dissertation for the Degree of Doctor of Philosophy in Population Genetics at Stockholm University to be publicly defended on Wednesday 5 June 2019 at 10.00 in Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20. Abstract Natural selection will act on a given phenotype to maximize fitness in a particular environment, even if this would result in reduced fitness in other environments. In insects some of the strongest selection pressures act on timing life cycles to seasonal variation in environmental conditions, in order to maximize growth, reproduction, and to anticipate the onset of winter. Many temperate insects survive winter by entering a pre-programmed state of developmental arrest, called diapause. The decision to induce diapause is predominantly based on measuring day length. Populations have adapted to latitudinal variation in photoperiod, thereby synchronizing with local seasonal variation. However, there is no general understanding of the genetic basis for controlling diapause induction, maintenance and termination. In this thesis I aimed to gain a better understanding of the genetic basis underlying variation in the induction decision, as well as to gain insights into gene expression changes during diapause in temperate butterflies. I started by revealing local adaptation in the photoperiodic response of two divergent populations of Pieris napi (Paper I). I found that variation in diapause induction among populations of both P. napi and Pararge aegeria showed strong sex-linked inheritance in inter-population crosses (Paper I and II). The genome-wide variation across populations was relatively low in both species. However, there was strong divergence in genomic regions containing the circadian clock genes timeless and period in P. aegeria, and period, cycle, and clock in P. napi. The genetic variation in these specific regions segregated between diapausing and direct developing individuals of inter-population crosses, showing that allelic variation at few genes with known functions in the circadian clock correlated to variation in diapause induction (Paper II and III). Furthermore, I investigated the transcriptional dynamics in two tissues (head and abdomen) during diapause (Paper IV). Already at the first day of pupal development there are on average 409 differentially expressed genes (DEG) each up and down regulated between the direct development and diapause pathways, and this increases dramatically across these formative stages to an average of 2695. Moreover, gene expression is highly dynamic during diapause, showing more than 2600 DEG’s in the first month of diapause development, but only 20 DEG’s in the third month. Moreover, gene expression is independent of environmental conditions, revealing a pre-programmed transcriptional landscape that is active during the winter. Still, adults emerging from either the direct or diapause pathways do not show large transcriptomic differences, suggesting the adult phenotype is strongly canalized. Thus, by integrating whole-genome scans with targeted genotyping and bulk-segregant analyses in population crosses, I demonstrate that adaptive variation in seasonal life cycle regulation in the two butterflies P. napi and P. aegeria both converge on genes of the circadian clock, suggesting convergent evolution in these distantly related butterflies. Moreover, the diapause program is a dynamic process with a distinct transcriptional profile in comparison to direct development, showing that on a transcriptome level diapause development and direct development are two distinct developmental strategies. Keywords: diapause induction, adaptation, genomics, transcriptomics. Stockholm 2019 http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-168042 ISBN 978-91-7797-719-3 ISBN 978-91-7797-720-9 Department of Zoology Stockholm University, 106 91 Stockholm FUNCTIONAL GENOMICS OF DIAPAUSE IN TWO TEMPERATE BUTTERFLIES Peter Pruisscher Functional genomics of diapause in two temperate butterflies Peter Pruisscher ©Peter Pruisscher, Stockholm University 2019 ISBN print 978-91-7797-719-3 ISBN PDF 978-91-7797-720-9 Cover image is copyright of Julie Horner. http://www.hornerartstudio.com Printed in Sweden by Universitetsservice US-AB, Stockholm 2019 The thesis is based on the following articles, which are referred to in the text by their Roman numerals: I. Pruisscher, P., Larsdotter-Mellström, H., Stefanescu, C., Nylin, S., Wheat, C. W., & Gotthard, K. (2017). Sex-linked inheritance of diaPause induction in the butterfly Pieris napi. Physiological Entomology, 42(3), 257-265. II. Pruisscher, P., Nylin, S., Gotthard, K., & Wheat, C. W. (2018). Genetic Variation underlying local adaptation of diaPause induction along a cline in a butterfly. Molecular ecology, 27(18), 3613-3626. III. Pruisscher, P., Nylin, S., Wheat, C. W., & Gotthard, K. (2019). A chromosomal block containing clock genes associates with Variation in diaPause induction. Manuscript. IV. Pruisscher, P., Lehmann, P., Celorio-Mancera, M., Nylin, S., Gotthard, K., & Wheat, C. W. (2019). TranscriPtomic Profiling of PuPal diaPause in the butterfly Pieris napi. Manuscript. Candidate contributions to thesis articles* I II III IV ConceiVed the study Substantial Minor Substantial Significant Designed the study Substantial Significant Substantial Significant Collected the data Substantial Significant Substantial Minor Analysed the data Substantial Substantial Substantial Substantial ManuscriPt preParation Substantial Substantial Substantial Substantial * Contribution ExPlanation Minor: contributed in some way, but contribution was limited. Significant: ProVided a significant contribution to the work. Substantial: took the lead role and Performed the majority of the work. I am also a co-author in the following articles that were written during my doctoral studies, but are not included in this thesis: Hill, J.A., Neethiraj, R., Rastas, P., Clark, N., Morehouse, N., de la Paz Celorio-Mancera, M., Keehnen, N. P., Pruisscher, P., Cols, J.C., Dircksen, H., Meslin, C., Sikkink, K., ViVes, M., and Wheat C.W. (2019). CryPtic, extensiVe and non-random chromosome reorganization reVealed by a butterfly chromonome. Science Advances in press. Lehmann, P., Pruisscher, P., Koštál, V., Moos, M., Šimek, P., Nylin, S., Agren, R., Väremo, L., Wiklund, C., Wheat, C.W. and Gotthard, K. (2018). Metabolome dynamics of diaPause in the butterfly Pieris napi: distinguishing maintenance, termination and Post-diapause Phases. Journal of Experimental Biology 221 (2), jeb169508 Lehmann, P., Pruisscher, P., Posledovich, D., Carlsson, M., Kakela, R., Tang, P., Nylin, S., Wheat, C.W., Wiklund, C., and Gotthard, K. (2016). Energy and liPid metabolism during direct and diaPause deVelopment in a pierid butterfly. Journal of Experimental Biology 219: 3049-3060. Stålhandske, S., Lehmann, P., Pruisscher, P., and Leimar, O. (2015). Effect of winter cold duration on spring Phenology of the orange tiP butterfly, Anthocharis cardamines. Ecology and Evolution 5: 5509–5520. SterVander, M., Illera, J. C., KVist, L., Barbosa, P., Keehnen, N. P., Pruisscher, P., Bensch, S., and Hansson, B. (2015). Disentangling the comPlex evolutionary history of the Western Palearctic blue tits (Cyanistes spP.) – phylogenomic analyses suggest radiation by multiple colonization events and subsequent isolation. Molecular Ecology 24: 2477–2494. CONTENTS INTRODUCTION ........................................................................................................................ 10 Local adaptation ................................................................................................................... 10 Genetic basis of local adaptation ......................................................................................... 10 Diapause induction and the circadian clock ........................................................................ 12 Diapause is a process ............................................................................................................ 12 The study system................................................................................................................... 13 OBJECTIVES OF THIS THESIS..................................................................................................... 14 METHODS ................................................................................................................................. 15 MAJOR FINDINGS AND CONCLUSIONS.................................................................................... 16 Photoperiodic response ........................................................................................................ 16 Mode of inheritance ............................................................................................................. 17 Candidate genes for diapause induction ............................................................................. 17 Gene expression differences between the pathways .......................................................... 20 Transcriptomic profiling of diapause. .................................................................................. 21 The end-product of two alternative developmental pathways .......................................... 21 Concluding remarks .............................................................................................................. 21 REFERENCES ............................................................................................................................
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