On Taxonomically Restricted Genes as They Relate to Translation

All extant life converts nucleic acid information to amino acid through protein synthesis. At the same time, genomes are constantly undergoing microevolutionary processes resulting in functional genetic diversity through myriad molecular mechanisms. In this dissertation, I consider the causes and consequences of transfer RNA gene proliferation in eukaryotic species with an emphasis on the role of sex therein. Classically, hypotheses on translational selection and co-evolution of tRNA copy number and codon usage have been invoked to explain the maintenance of tRNA gene duplicates. In contrast, I demonstrate translational conflict between unbiased codon usage of recently evolved genes and the evolving tRNA gene complement.Through comparative genomic analysis, I uncover an unexpectedly rapid rate of tRNA gene turnover across 60 million years of eukaryotic evolution. While new tRNA genes emerge continuously, population genetic analyses determine only a minority of tRNA genes are under directional selection. I empirically investigate the signficance of individal tRNA gene copies through small RNA sequencing of reproductive tissues. By comparing expression, fragmentation, and nucleoside modification patterns of individual tRNA copies, I demonstrate that selection of sex-biased functions likely underlies the maintenance of recently duplicated tRNA copies. I then study translational error through computational proteomic analysis of gonadal peptides and present evidence of equivalent mistranslation error rates between optimal and non-optimal codons. Together, I present a model of eukaryotic tRNA repertoire evolution in which nearly neutral processes, sexual selection, and directional selection together effect tRNA functional and copy number variation in metazoans. These findings expand our understanding of how origination time and sex differences affect the evolution and function of eukaryotic non coding RNA gene families. Thus, in addition to multiple tRNA copies supporting translational efficiency, new isodecoding and isoaccepting tRNA copies and their fragments can contribute to maximizing the fitness of each sex.