Abstract
Transcriptional regulation facilitates the emergence of unique phenotypes from shared genomes. While age and tissue differences require heterogeneous expression of the same genome within an individual, sex differences require heterogeneous expression of shared autosomal genes between individuals. The regulation of gene expression is the result of past selection, yet this regulation itself alters how selection acts upon genes. While evidence suggests that differential gene expression influences rates of evolution at the gene sequence level, there remain several questions. Much work has focused on differential gene expression, yet how other modes of transcriptional regulation, like alternative splicing, interact with differential gene expression to shape underlying genetic evolution is less clear. Further, factors of sex, age, and tissue shape transcriptomes, and while studies have investigated the effect of each factor on molecular rates of evolution, few studies have considered these factors together. Finally, the mode of selection that drives expression-dependent rates of evolution is currently contested, with stronger positive selection and weaker purifying selection both posited as mechanisms underlying different rates of evolution.
In this dissertation, I characterize patterns of differential expression and differential splicing with respect to sex, age, and tissue. Further, I test the relationship between differential gene expression and rates of evolution with the goal of interpreting the modes and strength of selection underlying gene sequence evolution. Using four species of lizards in the genus Sceloporus, I sequence multiple tissues, ages, and sexes to measure patterns of differential gene expression/splicing as well as measure rates of sequence variation between single-copy orthologs. In my first chapter, I find that differential gene expression and differential gene splicing occur together less often than expected, and while genes with sex- and age-biased expression tend to be highly tissue-specific, genes with sex- and age-biased splicing do not differ from unbiased genes in tissue-specific expression. While differential expression and differential splicing in sex- and age-biased genes do not appear to relate to variation in nucleotide diversity, I find evidence of higher nucleotide diversity in tissue-biased differentially expressed, but not spliced, genes when compared to unbiased genes. In my second chapter, I find evidence of faster rates of evolution in sex-biased genes, relative to unbiased genes, in three species. However, whether male-biased genes or female-biased genes evolve more rapidly depends upon the species examined. I find that adult-biased genes tend to evolve more rapidly than neonate-biased genes or unbiased genes. Further, I find evidence of rapid evolution in genes expressed primarily in the liver and slow evolution in genes primarily expressed in the brain and muscle. Selection analyses suggest that positive selection may be driving faster rates of evolution in some contrasts of differentially expressed genes. Together, my work demonstrates how factors of tissue, age, and sex shape differential gene expression and differential gene splicing, indicating that differential gene expression can explain variation evolution in underlying gene sequence.
