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Selection for the Xmrk Oncogene in Xiphophorus Cortezi

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Selection for the Xmrk Oncogene in Xiphophorus Cortezi SELECTION FOR THE XMRK ONCOGENE IN XIPHOPHORUS CORTEZI A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy André A. Fernandez August 2008 2 This dissertation entitled SELECTION FOR THE XMRK ONCOGENE IN XIPHOPHORUS CORTEZI by ANDRÉ A. FERNANDEZ has been approved for the Department of Biological Sciences and the College of Arts and Sciences by ___________________________________ Molly R. Morris Associate Professor of Biological Sciences ___________________________________ Benjamin M. Ogles Dean, College of Arts and Sciences 3 ABSTRACT FERNANDEZ, ANDRÉ A., Ph.D., August 2008, Biological Sciences SELECTION FOR THE XMRK ONCOGENE IN XIPHOPHORUS CORTEZI (142 pp.) Director of Dissertation: Molly R. Morris This dissertation examines sexual selection as a mechanism underlying the continued evolutionary maintenance of the Xmrk (Xiphophorus melanoma receptor kinase) cancer gene within the Xiphophorus melanoma model. Additionally, I expand this animal model to include Xiphophorus nezahualcoyotl (Order: Cyprinodontiformes, Family: Poeciliidae) as a species capable of non-hybrid melanoma formation. I use the well-studied Northern swordtail, Xiphophorus cortezi, collected from six localities throughout its geographic distribution to address whether the pigment pattern from which melanomas form (spotted caudal, Sc) and/or the Xmrk oncogene responsible for melanomas within Xiphophorus are advantageous in the acquisition of mates. Specifically, I address the following questions: 1) Is there a relationship between male aggression levels and the Sc phenotype and/or Xmrk genotype within individual males; 2) Does male aggressive response differ based upon the presence of the Sc phenotype; 3) Do females preferentially associate with Sc patterned males over non-Sc males or with larger Sc patterned males to size-matched males with smaller Sc patterns; and 4) Does the frequency of the Sc phenotype or the Xmrk genotype across the six populations influence male aggression levels or female mate choice decisions? 4 The results of mirror image trials found that the Sc macromelanophore pattern as well as the Xmrk oncogene (regardless of the presence of Sc) is correlated with increased aggression. In addition, Sc appears to function as a visual signal in male agonistic encounters because male aggressive response decreases when viewing their Sc image as compared with their non-Sc image. The frequency of Xmrk in males across populations ranged 0% to 87%. However, there was no difference in the aggression levels of males with Sc and/or Xmrk from each population thus the frequency of Xmrk within a population does not directly influence individual levels of male aggression. X. cortezi females from three populations, located in separate drainages that are genetically divergent, prefer to associate with Sc patterned males to non-Sc males. Moreover, X. cortezi females prefer males with an enhanced Sc pattern, which would occur during melanoma formation, to males with a reduced Sc pattern. However, unlike male aggression, there was variation in female preference for Sc males and it appeared to be influenced by the frequency of Xmrk in the population. Females from one population, which had the highest frequencies of Sc and Xmrk in females, discriminated against Sc patterned males and preferred to associate with non-Sc males. These results suggest there is a negative relationship between the strength of female preference for Sc and the frequency of Xmrk in females across populations. Because offspring with two copies of Xmrk have reduced fitness, and these offspring are more likely to occur in populations in which the frequency of Xmrk in females is high, females can increase their reproductive fitness by avoiding males with Sc (and therefore Xmrk) in these populations. 5 The findings of this dissertation have several important implications for the Xiphophorus melanoma model. First, non-hybrid melanomas occur in more Xiphophorus species than initially realized and may be more biologically relevant within Xiphophorus than melanomas formed via interspecific hybridization. Second, the Xmrk oncogene is associated with increased male aggression and thereby provides a competitive advantage for individuals in male-male competition. In addition, the macromelanophore patterns associated with the Xmrk oncogene can serve as signals in these male agonistic encounters. Third, female mate choice for the Xmrk associated melanin patterns plays an important role in the evolutionary maintenance of this oncogene. Finally, the relative frequency of Xmrk within each sex of a population does influence female mating decisions and is likely responsible for the continued polymorphism of Xmrk in all Xiphophorus that have retained this cancer gene. Collectively, the research presented in this dissertation demonstrates that sexual selection is important in explaining the persistence of Xmrk within this system. Approved: ____________________________________________________________ Molly R. Morris Associate Professor of Biological Sciences 6 To everyone and anyone who, over the last thirty-one years, made this document reality. 7 ACKNOWLEDGEMENTS Without question the first person I wish to acknowledge is my advisor and mentor, Dr. Molly R. Morris. The reason is simple: none of this would have happened without her giving me the opportunity to do so. Knowing what I know now about the process of graduate school (and the investment an advisor makes), I am truly amazed that she chose to take me on. I was five years removed from undergraduate education (with mediocre grades) and the only research experience I had was collecting data on primate foraging behavior in the field (I had never heard of a swordtail!). Yet, she read between the lines and believed in my potential to excel, which in turn has always led me to believe in myself. Thank you Molly. Thank you for allowing me the freedom to grow and develop as a scientist, yet always being there when I fell or needed guidance. I truly believe the latitude you give us, your students, is paramount to the success we attain. The integrative nature of this dissertation (sexual selection, evolutionary biology, and molecular biology of cancer) frequently pushed me beyond my training as a behaviorist and forced me to glean information and expertise from others with the Department of Biological Sciences at Ohio University. At the top of this list is Dr. Soichi Tanda. I am indebted to Dr. Tanda for his assistance and devotion in cracking the molecular code of this cancer gene (collectively, we ordered 53 custom primers before finally obtaining a primer set capable of screening for this cancer gene). Thank you for opening up your laboratory and imparting me with such great molecular techniques. Your optimism and humor in this endeavor proved vital in this last year. I would also like to 8 thank Dr. Matt White and Dr. Don Holzschu for numerous brainstorming sessions about this system over the last several years. I thank Dr. Joe Eastman and Dr. Bob Hikida for their willingness to help me with tissue histology and providing preservation materials. I would also like to thank Dr. Kathi Heffner (Dept. of Psychology) for taking the time to serve on my dissertation committee and discussing this project with me. Many people within the Department of Biological Sciences have helped me along the way and I would like to thank all of them. There are a few people that I must specifically mention for their persistent help. I have been fortunate enough to procure a few grants while at Ohio University and I certainly owe Linda Wise a BIG thank you for her bookkeeping of these grants accounts and her patience in ordering research supplies for this project. Susan Wagner-Svendsen thank you for constantly having a smile on your face with dealing with administration of these grants. I would like to thank Dr. Svendsen for allowing me to hole up in your space while studying for oral comprehensives and during the hours I babysat my daughter. There is also one student I wish to acknowledge, Eric McElroy. As a roommate, Eric’s intensity was infectious and I firmly believe the long days we logged during that year will be (and has been) instrumental to a successful academic career. I would like to thank everyone in the Morris laboratory for their assistance and support. I am grateful to Jason Moretz for his help with statistics early on and I wish I could have shared more time here with him. Oscar Rios-Cardenas, Carla Gutiérrez- Rodríguez, and Natalie Dubois for their tireless support and knowledge in the molecular laboratory. I want to thank Scarlett Tudor and Donelle Robinson for listening to my 9 oncogene ramblings in our office and for their efforts in collecting many of the fish in this dissertation. I would also like to thank the following undergraduates for their assistant in collecting data for this dissertation: Hiro Tanda, Katie Meadows, Lauren Toth, Jennifer Merzweiler, and Paul Crites. Throughout my tenure at Ohio University, my family has sacrificed spending time with me as my studies progressed. For me, as this immersion took place, the separation became easier and easier. This was not the case for them. Because the enticements of scientific investigations are unfamiliar to them, my persistent absences came with more and more bewilderment. I would like to thank all of them for saying they understand when I know they really didn’t. In my mind, such support is the definition of family. Saving the best for last, I am grateful for my wife and child, Lorie and Sadie Kathleen. Lorie, your unconditional patience, love, and support in this process has been inspirational. The up and downs we have witnessed, both professionally and personally, have been relentless. There is no greater shoulder to cry on or face to smile at than yours. I love you. Sadie thanks for being an excellent lab assistant. This research was funded by a National Institutes of Health NRSA pre-doctoral fellowship to A.
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