CHALLENGING TENETS OF SEX CHROMOSOME RESEARCH: OPTIONS ARE NOT LIMITED

Abstract

Sex chromosomes and what determines sex in an organism have been a topic of interest for decades. As such, the field has developed many tenets surrounding how they arise and evolve. In fish, transitions between sex determining systems occur at a much higher frequency than in other organisms. Here, I build on what is known about sex chromosomes in cichlid fishes and challenge some of these long-held tenets. Previously unknown sex chromosomes are discovered in the Lake Tanganyika tribes Cyprichromini and Tropheini, in the basal haplochromines, and in Chromidotilapia guntheri, a distant outgroup to the East African radiation. In the Cyprichromini, I show an unexpected transition from a ZW to an XY system on the same linkage group (LG). In the Tropheini, I present evidence for a high frequency of sex chromosome turnover and estimate a minimum of 14 turnovers in this tribe. The origin of the most common sex determining system in this tribe (XY-LG5/19) near the base of one of two major sub-clades of this tribe is dated to about 3.4 MY ago. Additionally, I observe variation in the size of one sex-determining region that suggests independent evolution of evolutionary strata in species with a shared sex-determination system. In the basal haplochromines, focusing on the genus Pseudocrenilabrus, I identify six new independent sex chromosome systems, including the first report of a cichlid sex determining system on LG12. I then quantify the rates and patterns of sex chromosome turnover in this clade and test whether some autosomes become sex chromosomes in East African cichlids more often than expected by chance. Finally, I identify an XY sex chromosome system on LG19 in the West African cichlid fish Chromidotilapia guntheri, in which the region of differentiation extends over less than 400 kb. I develop high-quality male and female genome assemblies for this species, which confirm the absence of structural variants, and which facilitate the annotation of genes in the region. The peak of differentiation lies within rin3, which has experienced several debilitating mutations on the Y chromosome. I suggest two hypotheses about how these mutations might disrupt endocytosis, leading to Mendelian effects on sexual development. This dissertation contributes >10 new cichlid sex chromosomes, suggests that chromosomes are not limited in their ability to become sex determining, and presents evidence of instances where previous theories have not held.