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1 Sex Determination and Interspecies Hybridization in Zebrafish Danio Sex determination and interspecies hybridization in zebrafish Danio rerio and pearl danio D. albolineatus Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Thomas Allin Delomas, M.S. Graduate Program in Environment and Natural Resources The Ohio State University 2018 Dissertation Committee Konrad Dabrowski, Ph.D., Advisor Macdonald Wick, Ph.D. Joseph Ottobre, Ph.D. 1 Copyrighted by Thomas Allin Delomas 2018 2 Abstract Sustainable management of fisheries and improvement of aquaculture production depends on an increased scientific understanding of fish physiology, nutrition, genetics, and ecology. With over 33,000 described fish species, and hundreds of these species being commercially fished or farmed, it is impractical to develop scientific resources and thoroughly investigate the biology of each species. One solution to this problem is the utilization of model organisms. The zebrafish Danio rerio is a widely used model organism in the larger experimental biology community. However, several areas of research need to be addressed for its utility to increase, particularly for fisheries and aquaculture research. First, rearing methods need to be improved, with an emphasis on larval and early juvenile stages. The sex determination system is controversial, but has been suggested to be polygenic. Finally, interspecies hybridization, which is a key tool in genetic improvement for aquaculture species, has not been thoroughly explored in the Danio genus. We present a series of studies addressing these areas of research in order to increase the utility of the zebrafish model system with an emphasis on applications to fisheries and aquaculture research. First, we designed and evaluated a rearing method utilizing a novel set of environmental parameters (3 parts per thousand salinity, high densities of live food, algal turbidity, 24L:0D photoperiod) from 5 to 21 days post- ii fertilization (dpf) that led to rapid growth rates (mean ± SD lengths of 19.4 ± 1.0 mm and 30.4 ± 1.5 mm at 21 and 42 dpf, respectively) and high fertility (232 ± 124 oocytes/female at 66 ± 3 dpf) (chapter 2). Next, we evaluated this protocol at temperatures close to the lower thermal limit for embryonic development (23°C) and observed no significant decrease in survival compared to a control group kept at optimum temperature (28.5°C) (chapter 3). We then utilized this rearing protocol to perform a series of investigations into the zebrafish sex determination system. First, we produced triploid zebrafish and confirmed previous studies that found triploid zebrafish to be all male. We then treated triploid zebrafish with estradiol (100ng/L) from 5 to 28 dpf, and found that both treated and untreated triploids were all male. Untreated diploid siblings were also all male while treated diploid siblings were 11% male. This demonstrates that triploidy acts downstream of estradiol to induce male development (chapter 4). Induced gynogenesis (inheritance of only maternal chromosomes) is a frequently used technique for investigating sex determination in fish species. Previous studies on gynogenesis in zebrafish reported inconsistent results and utilize irradiated zebrafish spermatozoa to induce embryonic development in zebrafish oocytes. This leaves open the possibility that rare, incompletely irradiated spermatozoa may cause gynogenetic progeny groups to be contaminated by biparental offspring. To address this methodological issue, we demonstrated that UV-irradiated common carp Cyprinus carpio spermatozoa activated embryonic development in zebrafish oocytes and that hybrids between zebrafish and common carp were inviable (chapter 5). We then used UV-irradiated common carp iii spermatozoa to induce gynogenesis in zebrafish. Out of 52 adult gynogens, only one was female. This is consistent with zebrafish having a polygenic sex determination system where inbreeding causes male development. Male gynogens and their biparental siblings were outcrossed to the same group of unrelated females. The families sired by gynogen males were more likely to be female biased than families sired by biparental males. This suggests that inbreeding induces male development through recessive and/or overdominant male-determining alleles (chapter 6). There are no studies investigating the sex determining systems of other Danio species, making it impossible to evaluate the evolution of sex determination in Danio. To address this gap, we investigated the sex determination system of pearl danio Danio albolineatus. We first performed a full-factorial mating and found that sex ratio varied between families from 5 to 100% male. Six breeding pairs were crossed twice and the sex ratios were not significantly different between the first and second crossings. Heritability was estimated at 0.89 (mean of posterior distribution) with a 95% credibility interval of 0.44 – 1.40. Together, these observations demonstrate that pearl danio has a polygenic sex determination system, and suggests that polygenic sex determination may be conserved between zebrafish and pearl danio. We then performed gynogenesis with pearl danio and the resulting gynogenetic families were strongly male-biased (91 ± 8% male). This suggests that inbreeding also induces male development in pearl danio (chapter 7). After observing the relationship between inbreeding and male development in zebrafish and pearl danio, we developed a hypothesis for why this may be an evolutionarily iv adaptive trait: male-biased sex ratios improve parental fitness under conditions of inbreeding through male-specific dispersal and investment in mate searching (chapter 8). Given the importance of interspecies hybridization to genetic improvement of aquaculture species, we explored whether zebrafish x pearl danio hybrids could serve as a model system for this technique. We first investigated the viability of both reciprocal crosses of zebrafish and pearl danio. Strongly asymmetric viability was observed between the two crosses, with zebrafish female x pearl danio male hybrids being viable and zebrafish male x pearl danio female hybrids being inviable past embryonic development. This is an example of “Darwin’s corollary to Haldane’s rule”, but the molecular mechanisms responsible for this phenomenon have not been empirically investigated, presumably due to the lack of a suitable model system. As such, we propose that this hybrid could serve as a suitable model for future mechanistic studies (chapter 9). We then investigated genetic influences on uniformity of growth in zebrafish x pearl danio hybrids. We found a recessive allele in zebrafish that caused hybrid offspring of zebrafish females homozygous for this allele to have dramatically higher uniformity of growth compared to those of other zebrafish females (mean coefficient of variation in length of 6 ± 1% compared to 21 ± 4% at 21 dpf) (chapter 10). Identification of the gene responsible for this effect and its mechanism of action could lead to similar genes being found in commercially important aquaculture species. This series of studies both advances the zebrafish model system for fisheries and aquaculture research and demonstrates use of the model system to address key issues in evolutionary biology and aquaculture genetics. v Dedication To Danielle vi Acknowledgments I would first like to thank my advisor, Konrad Dabrowski, for guiding me through this series of investigations. His advice and insight has been invaluable. I would also like to thank the members of my advisory committee, Macdonald Wick, Christine Beattie, and Joseph Ottobre for providing additional guidance and alternative perspectives on these studies. I would like to extend my sincere appreciation to Boris Gomelsky, who previously supervised my Master’s thesis research. The knowledge I gained while studying with him has provided the foundation for all of my work since. I would like to thank my fellow students at Ohio State University, both in the Aquaculture Laboratory and in the university as a whole, for frequent assistance and offering advice. Specific thanks are due to Mackenzie Miller, Megan Kemski, John Grayson, and Kevin Fisher. Finally, I would like to thank my family: my grandparents, Anthony and Barbara Spellman, Valeria and Jim Ratliff, as well as my parents Mark and Clare, for encouraging scientific pursuits throughout my childhood as well as their constant love and support. I would like to extend my utmost gratitude and appreciation to my wife, Danielle, for her love, support, and encouragement throughout my time at Ohio State University. vii Vita December 14, 1991 Born, Lexington, Kentucky, United States of America 2010 High School, The Gatton Academy of Mathematics and Science in Kentucky, Western Kentucky University 2012 B.S. Molecular, Cellular and Developmental Biology, University of Washington 2012 – 2013 Laboratory Technician, Department of Biosystems and Agricultural Engineering, University of Kentucky 2013 Analytical Scientist, KD Analytical, Inc. 2013 – 2015 Graduate Research Assistant, Division of Aquaculture, Kentucky State University 2015 M.S. Aquaculture / Aquatic Sciences, Kentucky State University 2015 – 2016 FAES Environmental Graduate Research Fellow, Ohio Agricultural Research and Development Center, The Ohio State University 2016 – 2017 Graduate Teaching Assistant, School of Environment and Natural Resources, The Ohio State University 2018 Presidential Fellow, The Ohio State University viii Publications
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