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Immunogenetic Variation Along the Latitudinal Gradient in Scandinavian Anuran Species

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Immunogenetic Variation Along the Latitudinal Gradient in Scandinavian Anuran Species Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1811 Immunogenetic variation along the latitudinal gradient in Scandinavian anuran species Evolutionary processes, demography and infection MARIA CORTAZAR-CHINARRO ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 ISBN 978-91-513-0662-9 UPPSALA urn:nbn:se:uu:diva-382092 2019 Dissertation presented at Uppsala University to be publicly examined in Zootisalen, Norbyvägen 14-18, Uppsala, Friday, 14 June 2019 at 13:00 for the degree of Doctor of Philosophy. The examination will be conducted in English. Faculty examiner: Senior lecturer Helena Westerdahl (Lund Universitet). Abstract Cortazar-Chinarro, M. 2019. Immunogenetic variation along the latitudinal gradient in Scandinavian anuran species. Evolutionary processes, demography and infection. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1811. 45 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0662-9. The evolutionary and demographic processes affecting how genetic variation is partitioned and distributed over large geographical scales is of fundamental importance for our understanding of how organisms may adapt to their environments. Northern peripheral populations generally have lower genetic variation and individuals in these populations may therefore face difficulties adapting to their local environment. At northern latitudes lack of genetic variation could be detrimental in face of newly emerging diseases as a result of anthropogenic actions and warmer climate in these areas. In this thesis, I explore genetic variation and the contemporary evolutionary processes affecting genes involved in the adaptive immune defense (Major Histocompatibility Complex; MHC) and the innate immune defense (AMP; Antimicrobial Peptides) over a large geographical gradient in anuran species (paper I, II and IV). I study signatures of historical selection on the MHC class II exon 2 and AMP (Temporin, Brevinin and Palustrin) sequences in the Signal Peptide and the Acidic Propiece domains (paper II and III). Finally, I investigate potential associations between specific MHC class II exon 2 alleles and a chytrid fungus infection (Bd) in common toads (Bufo bufo) (paper IV). The results reveal that genetic variation of MHC class II exon 2 decreases towards northern latitudes in R. arvalis and B. bufo and have been shaped by complex evolutionary processes (drift, selection, migration) affected by different demographic scenarios. On the other hand, AMP nucleotide variation is divergent among geographical areas, but there is no clear geographical pattern along the same gradient, suggesting diversifying selection as the main force shaping genetic variation. Finally, I found an effect of two specific MHC class II exon 2 alleles on survival in juvenile B. bufo when infected with Bd. In summary, my thesis unravels the complex patterns shaping genetic diversity at large scales. My results may guide conservation practices aiming to prevent amphibian mass mortality events on-going all over the world. Maria Cortazar-Chinarro, Department of Ecology and Genetics, Animal ecology, Norbyvägen 18 D, Uppsala University, SE-752 36 Uppsala, Sweden. © Maria Cortazar-Chinarro 2019 ISSN 1651-6214 ISBN 978-91-513-0662-9 urn:nbn:se:uu:diva-382092 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-382092) To Alberto, Axel, my parents and my family List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Cortázar-Chinarro, M., Lattenkamp, E.Z., Meyer-Lucht, Y., Luquet, E., Laurila, A., Höglund, J. (2017) Drift, selection, or migration? Processes affecting genetic differentiation and varia- tion along a latitudinal gradient in an amphibian. BMC Evolu- tionary Biology, 17:89 II Cortázar-Chinarro, M., Meyer-Lucht, Y., Van der Valk, T., Richter-Boix, A., Laurila, A., Höglund, J. Antimicrobial peptide variation along a latitudinal gradient in two Ranid species: AMP genetic variation is not associated with demographic processes. (Manuscript) III Cortázar-Chinarro, M., Meyer-Lucht, Y., Laurila, A., Höglund, J (2018). Signatures of historical selection on MHC re- veal different selection patterns in moor frog (Rana arvalis). Im- munogenetics, 70:6 IV Cortázar-Chinarro, M., Meurling, S., Schroyens, L., Siljestam, M., Laurila, A, Höglund, J. Latitudinal MHC variation and hap- lotype associated differential survival in response to experi- mental infection of two Bd-GPL strains in common toads. (Man- uscript) Reprints are made with permission from the respective publishers. Contents Introduction ..................................................................................................... 9 Research aims ........................................................................................... 11 Materials and Methods .................................................................................. 12 Study species and sampling collection ..................................................... 12 Rana arvalis (Paper I, II and III) ......................................................... 12 Rana temporaria (Paper II) ................................................................. 12 Bufo bufo (Paper IV) ............................................................................ 13 Sample collection ................................................................................ 13 Molecular Methods ....................................................................................... 16 DNA extraction (Paper I, II and IV) ......................................................... 16 Amplicon sequencing and library preparation (Paper I, II and IV) .......... 16 Other genetic markers (Paper I) ............................................................... 16 Experimental infections (paper IV) .......................................................... 17 Data Analyses ........................................................................................... 17 MHC and AMPs (Paper I, II, IV) ........................................................ 17 Statistical methods for measuring genetic variation and detecting selection (Paper I, II, III) ..................................................................... 18 Phylogenetic trees (Paper II, III) ......................................................... 19 Infection analyses (Paper IV) .............................................................. 19 Other analyses (Paper I) ....................................................................... 19 Results and discussion .................................................................................. 20 Genetic variation along latitudinal gradients (Paper I, II and IV) ............ 20 Diversity and Selection at the sequence level (Paper II and III) .............. 24 MHC Alleles associated with Chytrid fungus infection (Paper IV) ......... 25 Conclusions and future directions ................................................................. 27 Svensk sammanfattning ................................................................................ 28 Resumen en Español ..................................................................................... 31 Gracias, tack, thank you ................................................................................ 35 References ..................................................................................................... 41 Abbreviations MHC; major histocompatibility complex AMPs; Antimicrobial Peptides PBR; Peptide binding region Bd; Batrachochytrium dendrobatidis Introduction Decreasing richness in biological diversity along latitudinal gradients from tropical to extratropical areas is one of longest recognized patterns in ecology (Willig, Kaufman, & Stevens, 2003). Like most research in ecology and evo- lutionary biology, understanding patterns and mechanisms related to diversity along large-scale latitudinal gradients is quite challenging. Studies along en- vironmental gradients provide ample evidence for adaptive evolution, inferred from genetic divergence (Talarico et al., 2019). However, disentangling whether current patterns of genetic divergence are caused by drift, selection and/or migration is complicated by demographic history. One approach to study the role of evolutionary processes shaping contemporary genetic varia- tion contrasts diversity patterns of neutral markers with that at genes under targeted selection (Li et al., 2016; DeCandia et al., 2019). Vertebrates fight pathogenic infections using both the adaptive and innate im- mune system. The adaptive immune system, also known as the acquired im- mune system, is composed of highly specialized organs, tissues and systemic cells (Wood, 2006). The main cells of the specific immune system (e.g. lym- phocytes B and T) are able to synthetize glycoproteins (antibodies) and rec- ognize infinite diversity of antigens of single specificity tissue by entering through the bloodstream. Adaptive immune system, in contrast to innate im- mune system, usually clears infection and protects the host against reinfection with the same pathogen. One of the best understood adaptive molecules is the major histocompatibility complex (MHC class I and II). MHC molecules bind to specific antigens, which are presented to the TCR antigen-binding site of lymphocyted T cells (CD8+; MHC class I, CD4+; MHC class II) (Klein et al. 1989). Once the lymphocyted T cells are bound to a specific MHC molecule, the adaptive
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