The role of Y chromosomes in generating and maintaining intrasexual diversity

Project Summary Sex chromosomes are key drivers of intersexual diversity by harboring sex-limited genes and mediating sex- specific expression from the autosomes. In recent years, we have come to understand sex as a complex phenotype, with morphology and behavior that can be tremendously diverse not just between the sexes (intersexual diversity) but also within the sexes (intrasexual diversity). Intrasexual diversity has long been appreciated in evolutionary biology as the substrate for sexual selection, but the mechanisms by which sex chromosomes generate such intrasexual diversity are less known. The non-recombining nature of Y chromosomes subjects them to unique evolutionary processes, which have made them powerful regulators that drive differences in autosomal gene expression between the sexes. To determine the processes and mechanisms by which Y chromosomes also generate diversity within the sexes, we have developed the powerful Poecilia parae study system. Males of this fish are always one of five discrete morphs that differ substantially in size, color, and behavior yet live in the same population. We found these morphs are entirely inherited through highly diverged Y chromosomes. Our system uniquely provides the characteristics necessary for such research: (1) clear, diverse phenotypes that correspond to discrete Y-haplotypes in a homogenous autosomal background, (2) breeding lab populations for controlled studies of development, and (3) high-quality genomic resources. We will draw on this powerful new system to first identify how Y diversity alters gene regulatory networks across the autosomal genome (Aim1). While the non-recombining nature of Y chromosomes is generally thought to decrease the power of selection to generate adaptive diversity; the converse can also be true. Thus, we will identify how the unique processes of Y chromosome evolution can actually generate diverse supergenes (Aim2). Recent work in Drosophila has shown that Y chromosomes can alter heterochromatin structure across the rest of the genome by acting as “heterochromatin sinks”; thus altering autosomal gene expression. We will determine if heterochromatin sinks alter autosomal heterchromatin stochastically or in a targeted manner, generating intrasexual diversity (Aim3). The importance of understanding the mechanisms generating and maintaining diversity within the sexes has direct implications for our understanding of gene regulation and the developmental processes generating that diversity within the same population.