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Cellular/Molecular Analysis of Interspecies Sterile Male Hybrids in Drosophila

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Cellular/Molecular Analysis of Interspecies Sterile Male Hybrids in Drosophila Western University Scholarship@Western Electronic Thesis and Dissertation Repository 6-15-2017 12:00 AM Cellular/Molecular Analysis of Interspecies Sterile Male Hybrids In Drosophila Rachelle L. Kanippayoor The Unviersity of Western Ontario Supervisor Dr Amanda Moehring The University of Western Ontario Graduate Program in Biology A thesis submitted in partial fulfillment of the equirr ements for the degree in Doctor of Philosophy © Rachelle L. Kanippayoor 2017 Follow this and additional works at: https://ir.lib.uwo.ca/etd Part of the Biodiversity Commons, Biology Commons, Cell Biology Commons, Evolution Commons, and the Molecular Genetics Commons Recommended Citation Kanippayoor, Rachelle L., "Cellular/Molecular Analysis of Interspecies Sterile Male Hybrids In Drosophila" (2017). Electronic Thesis and Dissertation Repository. 4647. https://ir.lib.uwo.ca/etd/4647 This Dissertation/Thesis is brought to you for free and open access by Scholarship@Western. It has been accepted for inclusion in Electronic Thesis and Dissertation Repository by an authorized administrator of Scholarship@Western. For more information, please contact [email protected]. Abstract Over time, genetic differences can accumulate between populations that are geographically separated. This genetic divergence can lead to the evolution of reproductive isolating mechanisms that reduce gene flow between the populations and, upon secondary contact, result in distinct species. The process of speciation is, thus, what accounts for the multitude of species that contribute to the rich biodiversity on Earth. Interspecies hybrid sterility is a postzygotic isolating mechanism that affects the development of hybrids, rendering them sterile. A notable trend, known as Haldane's rule, describes how heterogametic individual hybrids (e.g. males in Drosophila) are more susceptible to sterility than homogametic hybrids. My objective was to describe the stage at which spermatogenesis fails in hybrids produced from three interspecies crosses in Drosophila. Identification of the stage of spermatogenic failure may inform the underlying basis of Haldane's rule. I found that chromosomes do not separate after meiosis I, leading to non-disjunction, and the formation of needle-eye sperm that is immotile but not dead. Secondly, sperm head length is aberrant in aged (6 days) sterile hybrid males, suggesting improper nuclear packaging, even with bi-allelic expression of sperm protamines. Third, individual sperm nuclei possess two sperm tails, with two undifferentiated, but active, mitochondria. Finally, I mapped for genetic factors that contribute to the formation of needle-eye sperm and identified possible candidate genes. Together, these studies highlight that spermatogenesis fails at a consistent stage in sterile hybrid males in Drosophila, leading to the formation of paired sperm that are unable to fertilize. My findings suggest that the genetic basis of hybrid sterility may be universal within the genus Drosophila. i Keywords Speciation, Postzygotic isolation, Spermatogenesis, Sperm, Testes, Meiosis, Protamines, Mitochondria, Sperm viability, Back-crossing, Next generation sequencing, Drosophila ii Acknowledgments I would like to extend my sincere thanks to all those who participated in my scientific growth. This thesis would not have been published if it weren't for the support of the following: First, to the Moehring lab members, both past and present: the original Moehring gang warmly welcomed me into the lab as a lowly technician and encouraged me to pursue graduate school. I can certainly say that I would not have survived all those late nights and long weekends in the lab without you all. So thank you to the following: Meghan Laturney, Vanda McNiven, Helene LaVasseur-Viens, Jessica Pardy, Christopher Dickman, Christopher Austin, Ryan Calhoun, Joshua Alpern, Trinh Nguyen, and Craig McNair. Thank you to current members of the Moehring lab. Your support to maintain my motivation to finish my thesis can never be thanked enough. I thank the following: Tabashir Chowdhury, Jalina Bielaska-Da Silva, Pria Mahabir, and Heather Ward. I wish you all the best of luck and I expect you all maintain the Moehring "epicness". Special thanks to my undergraduate students. Your patience with me and your smiles on the most trying of days provided me the strength to continue working. I am proud of what you all have become. To that end, I thank: Murad Rasheed, Joanna Mann, and Sarah O'Neill. I thank my advisors and the faculty members who continued to teach and mentor me since I first enrolled at Western as an undergraduate student. Special thanks to Dr Percival-Smith, who has been involved in every assessment of my student career (including my 4th year honours thesis). I can't imagine finishing off my graduate studies without you sitting across from me as my examiner. I would like to also thank the following: Dr Graham Thompson, Dr Susanne Kohalmi, Dr Brenda Murphy, Dr Robert Cumming, and Dr Bryan Neff. iii To Dr Anne Simon: thank you for pushing me to pursue a career in teaching. As a person, you are wonderful; as a teacher, you are inspirational. I have learned so much from you and I aspire to be as great as you are in educating the young minds of tomorrow. Finally, thank you to my supervisor, Dr Amanda Moehring. You took me into your lab on October 13th, 2009 and was finally able to kick me out in June 2017 (hopefully). You constantly challenged me to be a better scientist and to be a better person. My success throughout my entire graduate career is result of your constant guidance as my mentor. There are no words that will ever express how grateful I am that I was a part of your lab for so many years. It is bittersweet that I close this chapter of my life but I will continue forward with the wisdom and knowledge you've bestowed upon me. This thesis is dedicated to the memory of John Vincent. We really started something awesome. iv Table of Contents Abstract ............................................................................................................................... ii Keywords ........................................................................................................................... iii Acknowledgments ........................................................................................................... iiiii Table of Contents ................................................................................................................ v List of Tables .................................................................................................................... xi List of Figures ............................................................................................................... xxiii List of Symbols and Abbreviations ................................................................................. xiv 1 General introduction...................................................... Error! Bookmark not defined. 1.1 Postzygotic isolation ............................................................................................... 1 1.1.1 Extrinsic postzygotic isolation ....................................................................... 1 1.1.2 Intrinsic postzygotic isolation ........................................................................ 3 1.1.2.1 Hybrid inviability ............................................................................... 3 1.1.2.2 Hybrid sterility ................................................................................... 4 1.1.3 Trends for postzygotic isolation ..................................................................... 5 1.1.3.1 Hybrid sterility evolves before hybrid inviability ............................. 5 1.1.3.2 Haldane's rule .................................................................................... 5 1.2 Theoretical basis of hybrid sterility and Haldane's rule .......................................... 5 1.2.1 Dominance theory .......................................................................................... 5 1.2.2 "Faster-" evolution ......................................................................................... 8 1.2.2.1 Faster-male ........................................................................................ 8 1.2.2.2 Faster-X............................................................................................. 9 1.2.3 Meiotic drive .................................................................................................. 9 1.3 Genetic basis of hybrid male sterility ................................................................... 10 1.3.1 Improper chromosome pairing ..................................................................... 10 v 1.3.1.1 Speciation gene case study - meiotic pairing and Prdm9 ............... 11 1.3.1.2 Mismatched ploidy......................................................................... 11 1.3.1.3 Chromosomal inversion ................................................................. 12 1.3.2 Gene translocation and duplication .............................................................. 13 1.3.2.1 Speciation gene case study - transposition and JYalpha ................ 13 1.3.2.2 Speciation gene case study - odsH and novel gene functions in hybrids................................................................................................................... 14 1.3.3 Sterility due to genetic divergence at the same locus .................................. 14 1.3.3.1 Speciation gene
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