Selection for the Xmrk oncogene in Xiphophorus cortezi

FERNANDEZ, ANDRE 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: ____________________________________________________________