The Role of the Y-Chromosome in the Evolution of Autosomally Coded Traits

Recent work indicates that the Y-chromosome of the fruit fly Drosophila melanogaster can influence gene regulation on the autosomes and X chromosome. This newly discovered function of the Y has the potential to dramatically shape the regulatory evolution of numerous genes that reside throughout the genome; even for genes that code for both male and female traits. Given that the mechanism underlying the Y-linked influence on gene expression in D. melanogaster appears to exist in other independently evolved heterogametic sex chromosomes, the evolutionary implications of Y-linked regulatory variation (YRV) deserves to be explored. These implications include the potential for Y-chromosomes to facilitate the adaptive evolution of sexually dimorphic gene expression, and the potential for the Y to constrain evolutionary rates in both males and females (depending on the nature of the YRV effect). Unfortunately, the evolutionary implications of this potentially widespread and significant phenomenon have yet to be explored. My dissertation addresses this knowledge gap by determining the influence YRV has on the evolution of autosomally coded traits in D. melanogaster. First, we address the potential for selection to shape YRV by determining if YRV (i) exists within natural populations (i.e. where natural selection operates), and (ii) has any influence on male fitness-related autosomal traits. Second, we address if YRV can facilitate the adaptive evolution of sexually dimorphic gene expression by testing for the presence of Y-linked additive genetic variation. To this end, we investigate the physiological properties of select Y-chromosomes across multiple genetic backgrounds. Third, we address if YRV can constrain adaptive evolution for autosomally coded traits by employing artificial selection on replicate populations that contain either multiple Y-chromosomes (i.e. contain YRV) or only a single Y-chromosome (no YRV). The following studies present evidence that YRV does exist within populations where natural selection operates. We show significant levels of YRV on X-linked and autosomal immune gene expression in wild caught D. melanogaster from a single natural population. Furthermore, YRV effects on immune related genes show a significantly positive correlation to a male fly\u27s ability to fight an immune challenge (an important aspect of organismal fitness). Estimated physiological properties of YRV support previous interpopulation studies showing strong non-additive effect dependent on the autosomal genetic background with which Y-chromosome\u27s are paired with. Physiological epistasis can manifest as additive genetic variation on a population level, but our experimental evolution study suggest that YRV constrains rather than facilitates the evolution of the autosomal coded geotaxis behavior. Ultimately, this dissertation provides evidence that YRV has the potential to influence how autosomal traits evolve and that population level studies of YRV indicate a potential constraint to the adaptive evolution of autosomal traits. If these trends are common and YRV is a wide spread phenomenon, Y-chromosomes have the potential to influence how autosomal traits evolve