HJ Muller and the Relationship Between Sex Chromosome Degeneration and the Evolution of Dosage Compensation

Abstract

A lack of recombination in the heterogametic sex between parts or all of newly evolving sex chromosomes results in the gradual accumulation of deleterious mutations on proto-Y or proto-W chromosomes. This “genetic degeneration” is caused by several population genetic mechanisms. It can eventually lead to the loss of functionality and deletions of Y- or W-linked genes in species with male or female heterogamety, respectively, reducing the fitness of heterozygous XY males or ZW females. This creates selection to compensate for such degeneration. Contemporary studies of degeneration and dosage compensation are built on classical genetic work by HJ Muller, with molecular analyses of genomes and gene expression now revealing new details. We review these studies, integrating ideas about how degeneration and compensation evolve. We discuss whether these two processes evolve together, whether the initial changes involved in compensation occurred in individual sex-linked genes (“piecemeal”), and whether they were sex specific. We also discuss the idea that control of expression across larger chromosome regions reflects later changes, after increased expression of X- or Z-linked genes in both sexes favored reduced X expression in females (or Z expression in males with female heterogamety). We summarize the currently available empirical evidence and discuss difficulties involved in documenting the evolutionary changes that lead to the different types of dosage compensation, as well as limitations of the data for testing evolutionary hypotheses.