The Definitive Guide to the Evolutionary Biology of Sex


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What the Critics Say About Dr. Tatiana's Sex Advice to All Creation

Prospect Magazine - Mark Ridley

The end of men?
The Y chromosome is, in effect, cloned from father to son; and it is gradually decaying. In ten million years, human males may have ceased to exist.

Olivia Judson's Dr Tatiana and Steve Jones's 'Y'-two popular science books about the evolution of sex-are hugely different in style and content, but they both end up with the same question: are men on the way out? The ancestors of modern human beings all bred sexually, at least back to about two billion years ago. During that time, males have done half the breeding each generation. If you trace back the ancestry of your genes for the past two billion years, every one of those genes (or almost every one) has spent half its time occupying male bodies and half its time occupying female bodies. But will future generations continue to use sex when they breed?

Until recently, no one had asked the question. But in the past 25 years or so, it has become common in Darwinian circles and is now spreading into general culture. Dolly may have been the turning point. In Steve Jones's words, "Dolly the sheep-conceived without masculine assistance-had arrived. Her birth reminded half the population of its precarious position."

Olivia Judson writes about another piece of scientific work, from about the same time as Dolly, but less well known. It is the evidence that an obscure group of animals called bdelloid rotifers are "ancient asexuals." Many life forms are exclusive cloners, but their biological make-up suggests that we humans could not do without sex for long. Most exclusive cloners are microbes of one cell or less. Very few animals and plants are exclusive cloners. Moreover, the complex life forms that are exclusive cloners have been evolutionarily short-lived. Simple life forms can breed without sex, but complex ones that abandon sex soon seem to become extinct. Males, we can deduce, are necessary for some reason, in plants and animals.

But that deduction is rather spoiled by the bdelloid rotifers. Bdelloids are complex animals, and evolutionarily ancient; they have been around for 100m years or more. But no one has ever seen a rotifer male: they appear to be exclusive cloners. If so, as Judson says, "the ramifications are dramatic... if they can do without sex or males, maybe the rest of us can too."

Until about two years ago we only had negative evidence: bdelloids had not been seen to use sex. Now we have positive evidence of cloning in bdelloids. It comes from the difference between the two copies of each gene within a single body.

Each of us has two copies of each of the genes in our body-one copy from our father, the other from our mother. The two copies are either very similar, or identical. They have to be, because of the action of natural selection in the past. We have genes coding for all sorts of things including, for example, digestive efficiency. When a new version of a digestion gene arises-a version that is superior to the previous version-it slightly increases the chance that its bearer will survive and reproduce, relative to those with the normal digestion gene. The new version of the gene will then proliferate over time, until it eventually makes up 100 per cent of the copies of the gene in the population. That is why the maternal and paternal copies of each of your genes are much the same. They are descendants of superior genes, established by natural selection in the past.

The same cannot happen in a clonal population, such as a bdelloid rotifer. When a new superior version of a gene arises, it will initially be one of the two copies of that gene in a single organism. That organism will survive and breed better, and the gene proliferates. However, the cloned offspring of the mutant organism are genetically identical to it. They also have one copy of the superior version of the gene, together with one copy of the old version of the gene. The process may continue until every member of the species is descended from the mutant bdelloid but still they will all have one copy of the superior version of the gene together with another copy of the previous, different version.

Whereas the two copies of a gene in a sexually bred individual are much the same, the two copies in a long-time cloned individual are very different. The copies of each gene in a bdelloid rotifer individual are, in fact, so different that we can be reasonably sure that bdelloids have had no sex for 100m years or so. The obvious question is, what is it about these creatures that enables them to survive without sex? No one knows, though Judson offers some thoughts.

Bdelloid rotifers are not the only creatures in which pairs of genes differ within an individual because of a past history of cloning. Indeed, it can even be seen in part of the human DNA: the Y chromosome (this is the "Y" of Steve Jones's book title). Chromosomes are the physical structures that contain our genes. Our cells contain 23 pairs of chromosomes. One of those 23 pairs consists of the sex chromosomes, which determine gender. The sex chromosomes come in two forms, X and Y. If you have two X chromosomes you are female; if you have one X and one Y you are male. The Y chromosome, therefore, is only found in men. The Y chromosome acts as a master switch that turns on male development.

The Y chromosome reproduces, in genetic terms, clonally. In females, the two X chromosomes shuffle their genes in the standard sexual manner. The X chromosomes reproduce just like any other chromosomes, and the two copies of any gene on the X chromosomes in a female body are very similar. But in male bodies, genes are not shuffled between the X and Y chromosomes. When a father produces a son, he passes on the same Y chromosome as he inherited from his father: that is, Y chromosomes are a clone.

The genes you inherit on all 22 non-sex chromosome pairs are very similar from your father and mother. But if you are male, the genes on your Y chromosome are very different from those on your X chromosome. This difference between X and Y genes shows that the Y chromosome is an "ancient asexual" within the human DNA. The Y chromosome passes from father to son in an immaculate patriline, uncontaminated by female genes. I said above that the genes in your body have spent half their ancestral time in male bodies and half in female bodies. If you are male, this is not true of the genes on your Y chromosome. They have occupied only male bodies for a long time.

The Y chromosome may tell us something about what happens to cloned DNA in human beings. During evolution, the Y chromosome has been shrinking. About 150-200m years ago it was similar in size to the X chromosome. In those days, the ancestral Y and X chromosomes each carried about 1,000 genes. The modern human Y chromosome has only 50 genes. The Y chromosome has shrunk at the rate of about five genes per million years. It has probably shrunk because sex is needed to maintain genetic information. Once DNA goes without sex, it starts to decay. The genetically cloned, evolutionarily shrinking, exclusively masculine Y chromosome is a sort of monument to the necessity of males.

We can make an apocalyptic, if uncertain, prediction. If the Y chromosome continues to lose 5 genes per million years, it will disappear completely in the next 10m years. By then, either some other gene must evolve to direct male development, or we must perfect cloning-or we become extinct. "The Y chromosome," says Jones, "is a remnant of a once mighty structure, which might in a few million years disappear."

The prospective evolutionary insecurity of males is about the only point of contact between Judson's and Jones's books. Both range widely. The father-son inheritance of Y chromosomes enables them to be used to trace male movements in the past few hundred thousand years, and male reproductive habits in the present. Jones describes this research lucidly, and with his characteristic dry humour.

'Dr Tatiana' is written in a highly individual style. The book is made up of a series of agony aunt columns. Each begins with a short letter from an animal about its sex life. 'Dr Tatiana' then replies and advises. This is a wittily executed device for popularising a broad range of natural history. The book is not concerned to argue a single theme, but some themes are there nevertheless. For instance, Judson likes to subvert gender stereotypes. Males and females are often thought to differ in competitiveness and in promiscuity. But 'Dr Tatiana' deals with queries from creatures in which females compete for males, and seek out opportunities for multiple partners.

'Dr Tatiana' is not the sort of book to read out loud at a vicarage tea party. Judson relishes the grosser details of reproductive natural history, and likes to trample on taboos. Thus, in iguanas, males need to ejaculate quickly if their coitus is not to be interruptus by a rival. "That is why young males masturbate when they see a girl go by. Wanking reduces the time they need to ejaculate during sex." The male crab spider, by contrast, "is a great lover: he goes in for bondage, tying the female down (lucky her!) before making love." In the little brown bat, "anonymous males creep through vast winter roosts, raping females (and even males) who are hibernating." Scorpionflies sometimes steal food, including food that will be offered in courtship, from spiders. A spider's web can be dangerous. "Tip: if you're a boy scorpionfly, you'll have a big, bulbous penis. If you're in a spider's larder and the owner tries to stop you, whack her with your member and she'll back off. Girls, if you find yourself in this predicament, the best bet is to head butt the poor spider."

Those quotes may be an appetiser, or a warning. I liked the liberated style, together with the word-games and the poetic allusions. There is artistry in 'Dr Tatiana'. However, I can imagine-indeed, I have already learned-that some readers will like it less. Sticklers for scientific propriety will denounce it as anthropomorphic. Sticklers for political propriety will denounce it as incorrect. You cannot please everyone.

I write on the feast of the immaculate conception. This theological mystery had a chequered history until it was propounded as dogma on 8th December 1854. Nearly 150 years later, the theological mystery has become a biological one. We know something about the fate of cloned DNA-it seems to survive in bdelloid rotifers, but not in the Y chromosome. But our understanding of those facts is poor, and we still cannot explain why sinful reproduction prevails in so much of earthly life.