Evolutionary interactions between sex chromosomes and autosomes

The sex chromosomes offer a genetic apparatus involved in the sex determination in many dioecious organisms. There can be heterogametically defined males and homogametically defined females (the X–Y systems, e.g. humans and Drosophila) or vice versa as heterogametically females and homogametically males (the Z–W systems, e.g. chickens and silkworms). The origin and evolution of sex chromosomes has been a classic topic in evolutionary genetics that has led to many interesting observations and various theories with predicting powers. From a retrospective view, three stages of pursuit with respect to the evolution of sex chromosomes have provided much progress in understanding of the process, patterns, and evolutionary forces involved. In the first stage, attention was paid more often to the member of the sex chromosomal pair with genetically suppressed recombination, Y and W. It was proposed that these highly diverged, often degenerate, chromosomes originated from autosomes (Muller 1932; Ohno 1967; Charlesworth 1978, 1991; Lucchesi 1994), with mounting evidence recently from various genetic and genomic comparisons (Charlesworth and Charlesworth 2000). In the second stage, an active exploration examined the evolutionary changes that occurred on the X chromosome. For example, the rapid-X hypothesis, with its evolutionary dynamics that interpret the rapid change of X-linked genes (Charlesworth et al. 1987), explained whether or not sexual antagonistic mutations prefer an X-linked environment (Rice 1984). These two stages of exploration gave insight into the process and mechanisms of chromosomal evolution. Since several reviews (e.g. Vicoso and Charlesworth 2006; Ellegren and Parsch 2007; Ellegren 2011) provide clear overviews of these major lines of research, we will not simply repeat what these reviews have already summarized but will focus on the discussion of a new picture that is recently emerging in a third stage of sex chromosome evolution research: the interaction between sex chromosomes and autosomes. Whereas investigations based on the specific biology of sex chromosomes gave exciting insight and generated valuable data about the evolution of sex chromosomes, this third stage of research— exploring the interaction between coevolving sex chromosomes and autosomes—started a decade ago when a directional copying process through retroposition was observed (Betran et al. 2002). The central question raised was no longer how the two members of the sex chromosome pair and the genes encoded in them evolve by themselves, or how the sex chromosomes affect each other during evolution. The new question is whether or not the sex chromosomes and autosomes directly affect each other over evolutionary timescales. In other words, how is the evolution of the entire genome determined by evolutionary interactions between the sex chromosomes and autosomes? Three questions were derived from this newly defined problem: (1) what is the global genome-wide pattern associated with this interaction process? (2) How does the evolution of sex chromosomes globally change the gene content across the whole genome? (3) What is the evolutionary mechanism that underlies sex chromosome–autosome interactions? The pursuit of these questions presented a new angle to view, together, sex chromosome and genome