Will X be the only factor?

Brian Charlesworth rejects alarm at the degeneration of the Y chromosome.

Development as a male in most mammals is triggered in the early embryo by a signal from a gene, Sry, located on a particular chromosome, the Y, found only in males. The Y has a partner chromosome, the X, that is present in double dose in females but in one dose in males. Males receive their Y chromosome from their father and their X from their mother. Females receive one X from their father and one from their mother. Similar arrangements are found in many other groups of animals, and even plants.

Although the X and Y chromosomes come together as a pair during the cell divisions that precede the formation of sperm, they largely fail to exchange bits of themselves in the process known as crossing over. For all other chromosomes, the single copy that ends up in an egg or sperm is a mosaic of maternally and paternally derived material. This shuffling of genetic material between mother and father is the essence of sexual reproduction. The Y in effect lacks sex, and most of the genetic material on the Y is cut off from exchange with the X. There are, however, some genes shared by the X and Y in humans that indicate the common evolutionary origin of these two chromosomes, probably about 250 million years ago.

The X is a typical chromosome, carrying more than 1,000 different genes.

The Y lacks nearly all of these, and contains only 100 or so genes, most of which are involved in sperm function, although it is still a gigantic DNA molecule like other chromosomes. The Y is therefore often described as "degenerate". This degeneracy is probably a result of its, in effect, asexual mode of inheritance, which has reduced the ability of natural selection to maintain the functionality of most of the genes that were originally present on the Y. Mutations in the Y chromosome's DNA provide genetic markers that can be identified by molecular technology. The asexuality of the Y means that any combination of mutations carried on a Y chromosome remain together indefinitely, transmitted down generations from fathers to sons.

Bryan Sykes describes these facts with great gusto. He is professionally concerned with the use of genetic markers to trace the history of human populations. He starts by describing how the name Sykes is strongly associated with a particular genetic type of Y chromosome. This leads into a chapter describing the basic principles of genetics. While clear enough in outline, this is marred by errors of detail. For example, he attributes the discovery of crossing over to Arthur Sturtevant, but his name was Alfred and the discovery was made by Sturtevant's supervisor, Thomas Hunt Morgan.

Sykes describes the tangled history of the working out of the human chromosome complement, and the accumulation of evidence that the human Y chromosome carries the Sry gene required for development as a male. There are two chapters on the evolutionary significance of sex, and a discussion of why there are only two sexes, which overlooks the classic work of Geoffrey Parker on this topic.

The last few chapters indulge in wild speculations concerning topics such as the genetics of homosexuality and deviations from one-to-one sex ratios in human families. In the chapter "The rise of the tyrant", Sykes blames most of the disasters of history on male misbehaviour. He gives the impression that this is genetically encoded by the Y chromosome, ignoring the facts that sex differences in human behaviour are culturally dependent and that any genetic factors involved are likely to have nothing to do with the Y chromosome.

"Lifting the curse" discusses the degeneration of the Y chromosome. Sykes states that the asexual mode of transmission of the Y chromosome means that "it begins to decay because it cannot repair the damage inflicted by mutation". This is true in a broad sense, but Sykes makes the outlandish claim that the Y chromosome will continue to decay and that male fertility will drop to near zero in about 125,000 years, risking the extinction of the species. This is sensationalism, without any basis in the known causes of Y chromosome degeneration. It ignores the fact that the forces that have led to the present state of the Y chromosome have largely ceased to operate, since they require evolutionary interactions between large numbers of genes that have nearly all disappeared. There is no reason to suppose that selection will be ineffective in removing mutations to Y chromosomal genes that reduce male fertility. A good story has been spoilt by exaggeration and carelessness.

Brian Charlesworth is Royal Society research professor, Institute for Cell, Animal and Population Biology, University of Edinburgh.