The Human Y-chromosome: Evolutionary Directions and Implications for the Future of “Maleness”

Abstract

The human Y chromosome represents an iconic image of “maleness,” and mutation, deletion, or rearrangement of the Y often lead to attendance in infertility clinics. Its evolutionary history is however also one of gene loss, inversion, and heterochromatin accumulation. There is little argument that the Y chromosome once had the size and gene density of its partner, the X chromosome, and is thus now only a shadow of its former self. The question however revolves around whether we are observing the Y at a point on its way to oblivion, or whether it has evolved effective mechanisms to cling on to life indefinitely. There are two schools of thought: The first is that the Y has persisted for hundreds of millions of years and is going nowhere. It can, it is asserted, outsmart genetic decay without regular meiotic crossing over, and the majority of its genes show signs of evolutionary selection. Palindromic sequences along its length with near 100% identity ensure self-recombination. During its history, it has added at least eight different genes, some of which have expanded in copy number, and the Y has lost no genes since humans and chimpanzees diverged ~6 million years ago. The counterargument is that the Y chromosome is subject to higher rates of variation and inefficient selection and is degrading irreversibly. The Y chromosome in other mammals has undergone lineage-specific degradation and has already disappeared entirely in some rodent lineages, such as spiny rats and mole voles. The argument goes that there is virtually nothing left of the original human Y and that the added part of the chromosome is in fact degrading rapidly. An interesting aside to what should be really only a phenomenon of interest to evolutionary cytogeneticists is that the story often gets conflated in the popular press to assume that the alleged Y chromosome demise automatically means the demise of males. Fear not, it doesn’t. Males are here to stay, and the argument is about this strange looking chromosome alone. Everyone agrees that the Y has degraded significantly, it is now well established that it has evolved some clever mechanisms to put the brakes on. The prevailing question is how effective those brakes actually are. Even experts can’t agree and a straw poll at the 2011 International Chromosome Conference suggested an even split overall, but with more men favoring the “Y remaining” model and more women the “Y leaving” scenario.