Darwin's Island (18 page)

 

In his crossing experiments, Charles Darwin had no real idea of how and why his experimental subjects accepted or rejected particular kinds of pollen when he placed it on their female organs. He referred only to the ‘extreme sensitiveness and delicate affinities of the reproductive system’, which is poetic rather than persuasive. In fact, as in the cowslip and the tropical ginger, they make a test of kinship before deciding whether to accept a mate. The female parts judge the hopeful male cells by comparing their genes with their own. They reject any pollen grain if the similarity is too close.

The process is at work in the many hermaphrodites that insist on outcrossing. Like sperm, a grain of pollen contains but a single set of genes. Unlike the constituents of that potent liquid, the male sex cell from a flower must fight its way through a barrier of female tissue to reach the egg. To do so it grows a long pollen tube that penetrates into the appropriate part of its partner. Her protective layer bears the normal double complement of DNA. For her, to choose is simple: compare the pollen with her own tissues and if the two share too many genes, block it. For species that prefer to self-fertilise, the rule is relaxed or reversed.

For outcrossers, the system ensures that unrelated mates have the best chance of success. A new version of the identity cues carried by pollen is almost certain to succeed, for in its novelty it charms its way into the affections of all females, none of whom bear it themselves. As the generations go on, the new gene spreads - but it begins to lose its magic as more and more females inherit it and reject males with a matching copy. Each shift in male identity goes through the same process and in time a system emerges in which almost every individual has his or her own unique sexual calling card. That allows females to make decisions about the kinship of the hopeful males and to choose those most different from themselves. Other species delay that decision until later. The pollen is allowed to fertilise the egg, but matings with close kin are not allowed to develop further.

Animals - ourselves included - have a similar set of mechanisms, with a variety of genetic identity tests before sex is allowed. Some are obvious, while others are less so.

Simple familiarity can breed contempt. Unrelated Jewish infants brought up together in kibbutzim, or Asian children betrothed and made to live together when they are tiny, may prefer to avoid sexual contact when they grow up, and - in the latter case - are, after the arranged marriage, said to be less fertile and more liable to divorce than average. Brothers and sisters also tend not to fancy each other. Older sibs feel a stronger sense of aversion to their younger fellows than do the young to the old. The degree of kinship is the same, but the older child can be almost certain that the junior members of the household are the products of their own mother for they saw them cared for as babies. A younger sib, on the other hand, knows only that an older individual lives under the same roof - which could happen for other reasons. They are less repelled by the idea of sex with somebody who might not, after all, be a relative. It takes fifteen years of shared residence for a younger brother or sister to build up the erotic revulsion that an older member of the family can generate by watching a few months of childcare.

Social pressures play a large part in our marital patterns, but genes are involved too. Some are obvious - people do, after all, tend to marry someone of the same skin colour as themselves - but others are more subtle.

As a boy, I kept mice in my bedroom, a fad quashed because of the awful stench. At the time that was no more than a nuisance, but in fact the aroma of mouse urine was an introduction to a new world of sexual contact, through the nose. Quite unexpectedly, mice have more genes than we do. Almost all the extras are involved with the sense of smell. The genes that code for smell receptors - most of them decayed in the human race - are in full order. Mice have hundreds, which together can tell apart a vast diversity of scents. The animals choose both food and mates through the nasal passage.

Given the choice, an inbred laboratory female mouse prefers to mate with a male from a different line. So keen is she on a new swain that a pregnant female will resorb her foetuses to render herself available. Bedding soaked with male urine has the same effect. The females assess health as well as kinship. Their acute nostrils sniff out those who carry parasites and avoid them. Perhaps - as in the wormy sheep on the Isle of Soay - the healthiest males, with the most impressive statements of their fine condition, are less inbred.

Mice live in an aggressive sexual universe. Each male dominates a small patch in which he can monopolise the females, but their partners often hop over to a neighbour’s territory for a change. The male marks his boundaries with urine and females base their choice on the same stuff. The more urine there is and the less familiar it smells, the better. The males are forced to engage in liquid battles in which each tries to water down the offerings of his competitors. The females go for the most productive and most aromatic among them. So potent is the identity cue that even the human nose, feeble as it might be, can separate some mouse inbred lines by scent alone.

The perfume is based on a series of proteins, coded for by related genes in four different families, one of which has over a thousand members. Two others are expressed in a special organ with its own set of nerves, at the base of the nose. Not only do the proteins have a strong scent of their own, but they bind other male pheromones to make a cocktail of desire. The genes involved are highly variable. As a result - just as in flowers - females can avoid males with the same odour, and the same family history, as their own. Like them, they steer clear of potential swains with low variability in the smell-related proteins, perhaps because their reduced and inbred state makes them less suitable as fathers.

Primates, too, signal with scent - which is why the aftershave industry does so well. Marmosets and tamarins, small New World monkeys, send out chemical messages with dozens of constituents to mark their territories, to advertise when they are available, and to bond with their partners. A male’s brain lights up in response to female chemicals when she is most fertile. The largest response is in those parts of the marmoset brain associated in humans with emotion.

We smell, as any marathon runner soon finds out. Bloodhounds can sniff out individual identities and are confused by identical twins. Rats, too, can assess human kinship. The animals sniff for longer at an unfamiliar scent than at an odour that they have already experienced. Give them a sweat-soaked shirt and they can tell whether they have smelt it before. When tested with the scent of the brother of a familiar subject, they sniff less than when given a sample from a cousin. To rats, at least, we have an aromatic identity.

But can men and women, like rats, mice or marmosets, themselves identify the sweet smell of the opposite sex? The case is not proved. Many of the human genes for odour reception have rusted away, to leave fewer than half the number at work in mice, and we lack the special organ that is so sensitive to scent in other mammals (although a few of the genes that make it are still at work and will respond to mouse scents). Generations of students have sniffed T-shirts worn by women at different stages of the ovulatory cycle, with inconsistent results. In spite of the undoubted genetic differences that exist in the ability to taste certain chemicals it has been hard to obtain clear results on the role of scent in human mate choice.

Even so, some observations hint that - like dogs around lampposts - men and women do pass on romantic messages through the nose. Many perfumes contain synthetic musks of the kind used by monkeys or mice to choose a mate. One chemical, a relative of testosterone, has long been touted as a chemical messenger. The stuff is sold to farmers as ‘Boar Taint’ to test the sexual receptivity of sows. Some people can smell it while others deny that it has an odour of anything, but after several weeks of exposure even they begin to notice its presence and the number of relevant receptors in the nose goes up and up - and more in women than in men.

 

Mice, men and flowers have converged in their mutual distaste for sex with a relative, but how did such cues of identity evolve? There are intriguing similarities between the mechanisms of choosing a mate and those that fight off infection. An ancient tie between sex and disease may even be behind some of our own marital preferences.

All mammals, smelly or not, carry inherited identity cards on the surface of every cell. We cannot accept kidney transplants because our immune system compares the donor’s genes with our own, recognises the tissue as foreign and rejects it. The less related the source of the organ, the fewer the genes in common and the lower the chance of success, which is why brothers and sisters are better donors than are pairs of strangers. The identity system is based on a set of genes that sit close together on the DNA. They live in a section that codes for the many functions of the immune system, our prime defence against infectious disease, and, as an incidental, against the novel challenges presented by tissue transplantation. Each comes in many different forms, which means that vast numbers of combinations are possible.

Disease is a potent agent of natural selection. Individuals with the most diverse set of immune-system genes, and those with large numbers of rare variants, tend to fight off infection better than others. Mice and even fish prefer to mate with those least similar to themselves in immune identity, as a hint that the tie between sexual choice and disease resistance is ancient indeed. In the fight against infection, such diversity pays, for the next generation will have, thanks to sex, a new mix of defensive genes, confusing the parasites’ ability to evolve fast enough to evade our immune system. It hence pays to choose someone as different as oneself as possible.

As Darwin discovered, cowslips and other plants are very careful when deciding which pollen is acceptable, with a variety of devices to ensure that their reproductive parts stay free of cells from males physically similar to themselves. The erotic stink of mice does the same job and humans, too, may learn to avoid familiar kin. In truth, the sexual examination goes on well after the male cells arrive. Plants choose what pollen tubes are allowed to grow, and female insects may store the sperm of many males before deciding which should be allowed to travel further. Even after fertilisation, plants and mice are happy to abort a high proportion of their embryos, most of all those that arise from the attentions of a male relative.

The female reproductive system is a difficult and dangerous place for a sperm to find itself. Promiscuous mammals have longer vaginas than do those who stick to a few mates and make the male cells work harder to reach their goal. The vaginal tract is acid, too, and sperm do not much like that. In humans, of the millions implanted by a successful man, no more than a few hundred reach the neighbourhood of the egg, twenty or so make it to the point where they might be able to fertilise it and just a single cell gets in.

The smell of success lingers on after the sex act is over. Human sperm pick up and move towards chemical signals from the egg with the help of a gene that sits right inside the group that codes for smell perception. The complicated pore in the nose or the sperm cell membrane that picks up a single scent molecule, or a signal from the egg, each do more or less the same job and the two look remarkably alike - and, in a nod to their common heritage, some of the genes used by mice as they sniff the air to assess kinship by smell are also active in sperm. In an unexpected link between two sexual worlds, the sperm receptor also responds to the scent of lily of the valley and, given the choice, will swim towards it. Whether human eggs prefer to attract, or to allow entry to, sperm genetically different from themselves, we do not yet know.

Darwin’s work on the sex lives of plants has strayed into fields that would have shocked his contemporaries. His interest in their reproductive habits grew from his concerns about the effects of inbreeding in humans and on his own family in particular. Its influence is real, albeit less severe than he had predicted, and both plants and humans have evolved mechanisms that limit its effects. Faced with the same set of challenges, natural selection has come up with similar solutions in both kingdoms of life, which would not have surprised him (although he would, perhaps, be startled to discover that human sperm are attracted by the scent of a flower).

The great man’s concern about the possible damage done by cousin marriage to his own children was not justified. Of his sons, William became a banker and Leonard an army major. George was elected Professor of Astronomy and Francis Reader in Botany at Cambridge, while Horace set up as a scientific-instrument maker and was for a time mayor of that fair city. The naturalist’s offspring married into several eminent clans including those of Keynes and Huxley and - in spite of their progenitor’s concerns about inherited feebleness - have produced dozens of descendants eminent in science, medicine and the professions. They stand as living proof that intellectual aristocrats, unlike their botanical and blue-blooded equivalents, need not pay the price of keeping their biological heritage in the family.

CHAPTER V

THE DOMESTIC APE