by Steve Jones
Flowering plants have long been known to have sexual habits more inventive than our own. Charles’s grandfather Erasmus’s poem The Loves of the Plants is a work of science in two hundred pages of Arcadian verse. Many lines deal with the balance between male and female interests (‘Each wanton beauty, tricked in all her grace, Shakes the bright dew-drops from her blushing face; In gay undress displays her rival charms, And calls her wandering lovers to her arms’ - in other words, this species needs a pollinator). His descendant asked deeper questions in plainer prose. He found that many plants live in a reproductive universe that would have shocked the shepherds of Arcady. They have a system of choice that transcends the familiar preferences of one gender for its opposite. Most retain their original nature as hermaphrodites, with male and female parts in the same flower, but they span the range from obligate self-fertilisers to others that make an absolute demand for pollen from another individual. Many among the latter group have to ensure that they do not accept genes from their close kin, and have imposed additional and refined laws of sexual choice upon their mates.
The cross-fertilisation book was a first step in the scientific study of sex. Fifteen years earlier its author had noted that ‘We do not even in the least know the final cause of sexuality; why new beings should be produced by the union of the two sexual elements, instead of a process of parthenogenesis.’ Not much has changed. We are still not certain how the habit persists in the face of its obvious drawbacks in terms of cost, stress and more - in Dr Johnson’s famous words, its expense damnable, its position ridiculous and its pleasure fleeting. Why mate, when virgin birth ensures that your own genes have a guaranteed chance of survival? Parthenogenesis - virgin birth - guarantees that all the genes of those who indulge in it reach the next generation. It looks like the obvious solution but parthenogenesis remains rare - a few lizards and fish, and about one species of flowering plant in a thousand. For a hermaphrodite, a bout of sex with oneself also ensures that the DNA is not diluted with that of an unrelated individual. For creatures with separate males and females incest - sex with a close relative - is quite effective at keeping genes in the family, but that too is frowned upon.
Plants hint at the answer. Plenty among them have, like men and women, separate sexes. Some - like the strawberry or the dandelion - have gone to the opposite extreme for they are parthenogens and propagate themselves with shoots, roots or broken fragments. The majority of the flowering kinds have taken a lesser step towards asexuality for they are hermaphrodites that bear male and female functions on the same individual.
In spite of the chance they have for sex with themselves some hermaphrodites insist on exchanging genes with a stranger. Others in that situation are, in contrast, happy to self-fertilise and will accept genes from a different flower on the same individual, or evolve flowers with both male and female structures that can fertilise themselves. That pattern marks a real step towards the abandonment of sex.
Animals, too, have often tried to give up that habit. Some, like praying mantises and certain lizards, are true parthenogens, while a few such as snails and worms are hermaphrodites. Others go in for more bizarre forms of close copulation. The habits of mites would astonish any pornographer. A certain parasite of locusts gives birth to two types of male. The first clambers back into his mother and fertilises her. With their help she then produces a second brood, with a few males included - and those males then have sex with their sisters. In another mite, a mother has sex with her grandson, the scion of her own daughter, the daughter herself a child of the mother herself and a son. Other mites confine themselves to brother-sister pairs - but they copulate before they are born.
Darwin saw that, when it comes to sex, plants are more convenient subjects for experiment than animals. Self-pollination in hermaphrodites marks a biological indulgence more extreme than the matings between cousins that so concerned him, or between sons and mothers, fathers and daughters and brothers and sisters. He set out to explore how often it took place, what it did to the health of his subjects and, with luck, to learn a little about the importance of sexual reproduction in general.
Within a few months of starting work as a planned pollinator in the greenhouse at Downe he found that the effects of inbreeding could be dramatic. With the help of a botanical condom - a fine mesh to keep out insects - and a small paintbrush he could himself, like a bee, move male cells to the female parts of a flower and could arrange that the plant received its own genes, or those of another individual.
First, Darwin noted that certain species would self-fertilise, while others refused to do so even when obliged to try. Among those that did, he discovered - somewhat to his alarm - that the habit did damage later generations. His initial experiments were on toadflax, a common yellow-flowered weed. In the wild, outcrossing was the rule. In the greenhouse, he could force his subjects to self, and soon found a large, and unexpected, effect upon the next generation. The progeny of such crosses were smaller and less vigorous than were those of plants allowed to mate with another. At first he supposed that his inbred offspring were weakly because of some disease, or because they were grown in unsuitable soil. That was not so, for however well they were treated they stayed feeble. Darwin ran through a variety of species - carnations, tobacco, peas, monkey-flowers, morning glory, foxgloves and many other garden and wild flowers. With statistical help from Francis Galton he discovered that, almost without exception, those grown from crossed seed were taller, healthier and more productive than were those from self-fertilised. Some experiments went on for several generations, and the effects of sex with a relative got worse with time. The inbreds suffered most of all when life was hard: when they were crowded, had to compete with their outcrossed kin or were moved from the greenhouse to the rigours of the open air. The malign influence of selfing applied almost as much to species that went in for it in nature as to those that almost never did so.
Consistent as most of his results were, once or twice, out of thousands tested, the descendants of a self-fertilised individual were healthy and vigorous. Sometimes they even outgrew their competitors. A particular selfed morning glory (a species normally damaged by inbreeding) he referred to as ‘Hero’ because its line flourished under that mode of reproduction. Why, he did not understand.
Even so, in most plants in the wild, sex with a close relative appeared to be impossible, an expensive error or - at best - a doctrine of last resort. The implications for humans were, perhaps, alarming.
Darwin’s views were, we now know, too inflexible. Almost all hermaphrodite plants have at least the potential to fertilise themselves and many do so as a matter of course (he also denied the importance of selfing in animals and was again mistaken: I myself once worked on hermaphrodite slugs, who manage quite well with sex within their own skins). Only about one in five hermaphrodite plants prefers to self as a general rule. Others that normally outcross will self when no alternative is available and only a minority avoids the habit altogether. The notion that grew up in the century or so after his book that plants could be divided into two distinct types based on sexual habits is wrong. In fact, they go from obligate selfers to determined outcrossers, but most are happy to adopt either practice as conditions change. Some shift from sexual to asexual in different places or as the seasons move on. For others selfing is a side-effect of sex, a kind of green onanism when a bee, as it flits from flower to flower, fertilises one flower with pollen from another on the same individual.
The decline in fitness of self-fertilised individuals and the occasional appearance of healthy lineages both emerge from the simple rules of inheritance (which were not known to the nineteenth century) and from the existence of large amounts of hidden genetic damage in most plants and animals. A hermaphrodite that bears two different versions of a particular gene - for example, a pea in which the DNA that codes for seed shape has the instructions for round seeds paired with another set for wrinkled - will, after self-fertilisation, produce half the next generation with the ro
und-wrinkled mix, a quarter with round alone and a quarter with just wrinkled. If they are again selfed, the pure round and pure wrinkled plants will have offspring identical to themselves while those with both kinds of instruction will repeat the proportions that emerged in the previous generation - a quarter pure round, a quarter pure wrinkled and the remainder with a single copy of each variant. As selfing goes on, a smaller and smaller proportion of the population retains both versions of the shape gene. Generations of such crosses hence lead to the emergence of ‘pure lines’, within which every individual is identical: all with round seeds or all with wrinkled. The same is true for every other variant in each line. In time, each will contain different combinations of genes for seed shape, colour, height and so on.
To make a pure line is not easy, for if the original population contained hidden variants harmless in single dose but harmful in double (as many do), its descendants pay the price when such variants are exposed in double copy. The more damage is concealed, the smaller the chances of success. The effect can be spectacular. In loblolly pines, natives of the southern United States, just a fiftieth of eggs fertilised by pollen from the same plant survive. As a result it is almost impossible to make an inbred line.
Lines of genetically identical plants are at the centre of modern agriculture. Thousands have been produced for use as crops or as garden flowers. Wheat, rice, barley, tomatoes and more - all have their reproductive lives controlled by farmers and almost all are the descendants of a few survivors from vast numbers of inbred lines who paid a fatal price for the damaged genes hidden within their ancestors. The survivors were those who drew lucky in the sexual lottery. Darwin’s discussions with breeders told him that the first few generations of kin mating caused the effects to get worse and worse - because, we now know, more and more harmful genes emerge in double copy as time goes on. Now and again, as in the famous morning glory ‘Hero’, an inbred line wins because it inherits, by chance, genes that increase, rather than reduce, its ability to survive. Its descendants thrive and may, in time, be used in their millions on farms or in gardens.
Farmers, consciously or not, have built on that observation and the same is true in the wild. In some species, well-adapted inbreds emerge to cope with the horrors of Nature. Millions of identical individuals then fill the landscape. The advantages of self-fertilisation often depend on how predictable life may be. The practice is commoner when the struggle to survive involves starvation or bad weather, which come back more or less unchanged each year. Perhaps, by chance, a set of genes emerges that deals well with food shortage or with cold. It then pays to stick to that well-adapted combination rather than to mix it with other genes during a spasm of sex. Selfing is more frequent in cold and starved northern forests and when life is short or when few mates are available. For hermaphrodites whose pollinators are grounded by bad weather, or if the season is so bad that it becomes hard to make a decent flower, a shift to selfing also makes sense, for the choice is between an unhealthy brood or none at all.
If - as in the tropics - the main enemies are parasites or predators, who themselves use sex to shift their own tactics by scrambling up their genes, that tactic does not work. For a plant to stick to a single strategy is to play poker with the same hand each time against an opponent who reshuffles on each deal. Sooner or later the other player will draw an unbeatable combination, and the selfer will go bust.
The rules that apply to plants work for animals too. When - in an echo of the Down House experiments - wild mice are mated brother with sister in the laboratory and the offspring released into nature almost none survive. Inbred animals do not often die of obvious genetic disease, but their parenthood can much weaken them. Song sparrows on a small island off Canada’s west coast have been ringed for years and their pedigrees worked out in detail. Those born to close relatives are at more risk of death in bad weather than are other birds. The island of Soay, in the St Kilda group, is famous for its native sheep, which have been there since Viking times. The animals are filled with worms, and those with the heaviest burden suffer most of all when faced with a vicious Scottish winter. Lambs born to close relatives have more parasites, and are at more risk of death in storms, than others. Once purged with medicine, though, the inbred animals survive the tempest as well as do their outbred kin, as proof that the worms are to blame. The finches on the Galapagos also pay the price for sex with close relatives, as do wild shrews, red deer, seals, toads, bats and many other creatures.
Endangered species are, given the shortage of mates, at particular risk. Planned parenthood can help. The Florida panther was once on its last legs, with many animals plagued with kinky tails and undescended testicles because of the exposure of genetic damage in the tiny and inbred population that remained. In 1995, eight female Texas cougars (a related species) were introduced, and now the natives, with the help of their relatives’ genes, have fought off their tail and testicle problems and returned to genetic health. The situation in zoos is just as bad. A mere hundred or so Arabian oryx were left in the wild by the 1960s, and most were soon killed by hunters. Two males and a female were rescued, and a dozen or so additional individuals were already in captivity. The entire world population of two thousand individuals, domestic and nominally wild, now descends from those few founders - and the most inbred individuals still have fewer young than average.
If sex within the family is bad for plants and animals, what might it do to people? Many are convinced of its dangers and many societies try to limit the practice. Every one of the United States has some restriction on marriage between relatives and cousin marriage is a criminal offence in eight states and in a further twenty-two is at least illegal, although the rules are often ignored. An attempt to ban such alliances was defeated in Maryland as recently as the year of the millennium. In a nod to the eugenic agenda, Wisconsin restricts them to couples in which the wife or husband is infertile, or where the wife is over fifty-five. The traditions of particular groups can lead to a reluctant acceptance of difference; uncle-niece marriages are allowed in Rhode Island but only for Jews, and male Native Americans in Colorado are allowed to marry their step-daughters even if elsewhere the habit is, in spite of the lack of any shared genes, against the law. Europe is just as confused. In Cyprus the Church prohibits marriage between second cousins but in Belgium incest is not even mentioned in the statute books. Britain, too, forbids incest and even prohibits the - rare - sexual liaisons between grandfather and granddaughter. Sweden, in contrast, permits half-sibs - children with one parent in common - to enter into marital bliss should they wish. The nation has even considered the legalisation of wedlock between brother and sister.
It is, needless to say, impossible to carry out planned crosses with men and women, but Charles Darwin came up with another way to test the dangers of inbreeding. First, he tried to get questions about cousin matrimony included in the 1871 census. He pointed out that ‘the marriages of cousins are objected to from their supposed injurious consequences; but this belief rests on no direct evidence. It is therefore manifestly desirable that the belief should either be proved false, or should be confirmed, so that in this latter case the marriages of cousins might be discouraged.’ His request was debated in the Commons but thrown out as ‘the grossest cruelty’, for it would cause children to be ‘anatomised by science’ (and from a parliamentary point of view the issue was almost traitorous, for the Queen herself had wed her cousin). A query about ‘lunatics, imbeciles and idiots’ was allowed but was dropped for the next census a decade later as most people refused to answer it. Darwin was annoyed by his failure to persuade Parliament to ask a scientific question and complained about ‘ignorant members of our legislature’. His son George was even more caustic about ‘the scornful laughter of the House, on the ground that the idle curiosity of philosophers was not to be satisfied’.
George Darwin set out to build on his father’s work. From the records of Burke’s Landed Gentry and the Pall Mall Gazette, together with a circular s
ent to lunatic asylums, he worked out the frequency of cousin marriage in various groups. Such unions were, it transpired, twice as common among noblemen as among the proletariat. His enquiry to the superintendents of asylums as to how many of those in their care were the scions of related parents was, as they pointed out, unlikely to pay off because of the mental state of their charges. Even so, George found no increase in the level of inbreeding among the patients compared with that of the general population (even if the Deputy Commissioner in Lunacy for Scotland did assure him that most of his nation’s idiots were the children of relatives).
After his mixed success with lunatics, the young man went on to study the inmates of Oxford and Cambridge colleges. He chose the boat-race crews - ‘a picked body of athletic men’ - and asked how many had been born of cousins. After a correction for a falsified answer from the stroke of Corpus Christi College Cambridge, he found that there was indeed a slight shortage of such inbred individuals among top oarsmen compared with the general population. The same was true among sporting boys in the principal schools for the upper and middle classes. In both cases the numbers were small and the evidence not altogether persuasive.