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Immunocompetence and Parasitism in Hybrids of Cyprinoid Fish

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Immunocompetence and Parasitism in Hybrids of Cyprinoid Fish FACULTY OF SCIENCE Immunocompetence and parasitism in hybrids of cyprinoid fish Ph.D. Thesis VADYM KRASNOVYD Supervisor: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Department of Botany and Zoology Brno 2020 Bibliographic Entry Author: Mgr. Vadym Krasnovyd Faculty of Science, Masaryk University Department of Botany and Zoology Title of Thesis: Immunocompetence and parasitism in hybrids of cyprinoid fish Degree Program: PřF D-EKEB Ecological and Evolutionary Biology Specialization: PARA Parasitology Supervisor: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Faculty of Science, Masaryk University Department of Botany and Zoology Academic Year: 2020/2021 Number of Pages: 148 Keywords: Interspecies hybridization, cyprinoids, immune response, maternal ancestry, monogeneans, parasite community, heterosis effect, host-parasite interactions, coadaptation Bibliografický záznam Author: Mgr. Vadym Krasnovyd Přírodovědecká fakulta, Masarykova univerzita Ústav botaniky a zoologie Název práce: Imunokompetence a parazitismus u hybridů kaprovitých ryb Studijní program: D-EKEB Ekologická a evoluční biologie Specializace: PARA Parazitologie Vedoucí práce: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Přírodovědecká fakulta, Masarykova univerzita Ústav botaniky a zoologie Akademický rok: 2020/2021 Počet stran: 148 Klíčová slova: Mezidruhová hybridizace, kaprovité ryby, imunitní odpověď, mateřská linie, Monogenea, společenstva parazitů, heterózní efekt, hostitelsko-parazitické interakce, koadaptace Abstract Fish hybrids and their parasites represent interesting models for evolutionary ecology. The modified immune response, ecological plasticity, maternal ancestry and vigour of hybrid fish are supposed to impact the diversity and distribution of their parasites. In the study A, common bream (Abramis brama), roach (Rutilus rutilus) and their hybrids were investigated. Metazoan parasite abundance and prevalence were higher in parental species when compared to their hybrids. Temporal and spatial effects on the parasite distribution were analysed. The effect of maternal ancestry of hybrids on digenean and crustacean infection level was confirmed. Asymmetrical distribution of parental species-specific parasites in favour of roach-specific parasites in hybrids was discovered. The effect of interspecific hybridization on vigour, physiology and immunity of cyprinoid fish was investigated (study B). Generally, hybrids tended to express intermediate characters of these traits. Role of the heterozygote advantage for F1 hybrids was proposed. Maternal origin of the hybrids was suggested to be involved in the expression of some branches of non-specific immunity. The experimental monogenean infection in pure breeds of silver bream (Blicca bjoerkna) and common bream and F1 cross-breeds under the condition of similar frequencies of pure and hybrid genotypes was investigated (study C). Potential effect of the maternal origin of hybrids on monogenean abundance was tested. Each of pure species harboured specific monogenean fauna. Hybrids harboured all monogenean species specifically infecting one or the other parental species. Monogenean infection level especially that of Dactylogyrus specific to A. brama was low in hybrids. We found no obvious effect of the maternal origin of hybrids on monogenean abundance, which indicates that the mtDNA of hybrids is not an important predictor of host-specific monogenean infection. This may suggest that mitochondrial genes are not strongly involved in the coadaptation between monogeneans and their associated hosts. The asymmetry in the distribution of A. brama specific parasites and B. bjoerkna-specific parasites in hybrids suggests similarity in the molecular components of the immune mechanisms between hybrids and B. bjoerkna. In conclusion, the necessity for genomic studies focused on the genes involved in reciprocal genetic co-adaptations of host-specific parasites and their associated hosts is highlighted by this study. Investigation of inherited protective immunological mechanisms that limit monogenean infection may shed light on the asymmetry in the presence of host-specific parasites in hybrids. Abstrakt Hybridi ryb a jejich paraziti představují zajímavé modely v evoluční ekologii. Modifikovaná imunitní odpověď, ekologická plasticita, mateřský původ a vitalita hybridů ryb mohou ovlivňovat diverzitu a distribuci jejich cizopasníků. Ve studii A byli studováni cejn velký (Abramis brama), plotice obecná (Rutilus rutilus) a hybridi první filiální generace (F1). Abundance a prevalence mnohobuněčných parazitů byla vyšší u rodičovských druhů ve srovnání s jejich hybridy. Analyzovány byly časový a prostorový vliv na distribuci parazitů. Prokázán byl vliv mateřského původu hybridů na míru parazitární infekce korýšů a motolic. Byla zjištěna asymetrická distribuce parazitů specifických pro rodičovské druhy u hybridů ve prospěch parazitů specifických pro plotici obecnou. Byl studován vliv mezidruhové hybridizace na vitalitu, fyziologii a imunitu (studie B). Hybridi měli obecně tendenci vykazovat střední hodnoty většiny měřených parametrů. Podpořena byla hypotéze heterozygotní výhody hybridů F1 generace. Zaznamenán byl efekt mateřského původu hybridů na expresi některých linií nespecifické imunity. Ve studii C byla analyzována experimentální infekce zástupci taxonu Monogenea u linií Blicca bjoerkna (cejnek malý), A. brama a jejich F1 hybridů v podmínkách podobných četností čistých a hybridních genotypů. Testován byl možný vliv mateřského původu hybridů na abundanci monogeneí. Oba druhy, B. bjoerkna i A. brama, byly parazitovány hostitelsky specifickými zástupci taxonu Monogenea, u obou druhů byla zaznamenána podobná míra parazitární infekce. Hybridi byli parazitováni všemi druhy monogeneí hostitelsky specifickými pro B. bjoerkna nebo A. brama. Míra infekce zástupci taxonu Monogenea, zejména infekce druhy rodu Dactylogyrus specifických pro A. brama, byla nízká u hybridů. Nebyl prokázán vliv mateřského původu hybridů na abundanci monogeneí. Výsledky ukazují, že mtDNA hybridů není důležitým indikátorem infekce druhy taxonu Monogenea specifickými pro hostitele, což může naznačovat, že mitochondriální geny nejsou zapojeny do koadaptace specifických monogeneí a jejich asociovaných hostitelů. Asymetrická distribuce parazitů druhově specifických pro A. brama a druhově specifických pro B. bjoerkna u hybridů ukazuje na podobnost mezi molekulárními složkami imunitních mechanismů mezi hybridy a B. bjoerkna. Z práce vyplývá potřeba genomických studií zaměřených na geny podílející se na vzájemných koadaptacích specifických parazitů a jejich hostitelů. Studium dědičnosti obranných imunitních mechanismů limitujících infekci zástupci Monogenea může také osvětlit asymetrii v míre vnímavosti hybridů k hostitelsky specifickým parazitům. Acknowledgement First of all, I would like to express my deepest gratitude to my supervisor prof. RNDr. Andrea Vetešníková Šimková, Ph.D. for her kind help, patience with me, and support. I would like also to express my sincere gratitude to Lukaš Vetešník for his help and contribution during all of these years to this work. I would like to thank Pavel Jurajda and colleagues from the Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic (and the whole team involved) who kindly helped with fish sampling. Also, I would like to thank my friends, labmates and colleagues from Department of Botany and Zoology, Faculty of Science, Masaryk University for helping with the fish dissections. I am thankful to Markéta Ondračková for the opportunity to be involved in the several dissections and field trips to Germany. I want to thank Pavel Hyršl and Jiří Jarkovský for all of their help. I want to thank Peter Stuart for kind help with the English revision of the thesis. I am grateful for the opportunity provided to work in the Department of Botany and Zoology, Faculty of Science, Masaryk University. This thesis was funded by Czech Science Foundation, projects No. P505/12/G112 and No. P505/12/0375. In the end, I would like to thank my family and friends for keeping me motivated and keeping my “wheels rolling” even when it was extremely hard. The last, but not least, my sincere gratitude goes to my schoolteacher of biology and chemistry Bondar' Ludmila Yaroslavna, who was kind and patient enough to teach such a wild child as I was in the past. Original papers and contribution of the author to the papers included in the thesis Thesis includes 2 scientific papers and 1 manuscript under revision. Paper A Krasnovyd, V., Vetešník, L., Gettová, L., Civáňová, K., & Šimková, A. (2017). Patterns of parasite distribution in the hybrids of non-congeneric cyprinid fish species: is asymmetry in parasite infection the result of limited coadaptation? International Journal for Parasitology, 47(8), 471-483. Vadym Krasnovyd (VK) processed parasitological material, identified parasite species, performed mitochondrial identification of fish specimens. He was involved in the fish sampling and dissection and parasite collection. He prepared database. VK contributed to manuscript preparation. Paper B Šimková, A., Janáč, M., Hyršl, P., Krasnovyd, V., & Vetešník, L. Vigour-related traits and immunity in hybrids of evolutionary divergent cyprinid species: advantages of hybrid heterosis? (resubmitted to Journal of Fish Biology) VK was involved in the fish sampling and processing of material collected from fish specimens. He prepared database and partially participated on manuscript writing. Paper C Krasnovyd, V., Vetešník, L., & Šimková,
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