Sex is best when you lose your head

In 1853 the Reverend Frederick Morris, an opponent of Charles Darwin’s and a man with a Victorian sense of propriety, urged his parishioners to emulate the fidelity of a small bird called the dunnock. Be thou like the dunnock, he told them – the female and the male impeccably faithful to each other.

What would the Rev. Morris have made of the scandalous truth? Far from being monogamous, the dunnocks, from a Victorian point of view, have shockingly lax morals. The female dunnock often takes not one but two males as partners. The best a stern man of religion could say about dunnocks is that there’s no superfluous bump and grind when they mate – it’s strictly fertilisation business, over in 0.1 seconds. Fast enough to do it while your mother’s back is turned.

Tim Birkhead and his fellow evolutionary biologists, exploring the nature of sexuality across species from single-celled organisms to humankind, are the paparazzi of the science world. They travel to remote islands and put up with extreme discomfort in the hope of catching animals having sex with each other, and when they do, splash their names and their pictures over the pages of the science journals. It doesn’t always work out. Fiona Hunter and a colleague, later to expose what the mainstream media dubbed ‘penguin prostitution’ in the Antarctic, once watched a colony of fulmars on Fair Isle for 56 days on the trot, 18 hours a day, only to find the species relatively faithful: a mere 16 per cent of females had sex with a bird who wasn’t their partner, and there were no ‘illegitimate’ chicks. This isn’t a glamorous pursuit. Geoff Parker, one of the human heroes of Birkhead’s story, spent months with his face a few centimetres away from fresh cowpats, watching female dungflies being aggressively mounted by two males in turn. Sometimes the biologists witness scenes more disturbing than they had anticipated: Mats Olsson, observing the rape-like mating of the Lake Eyre dragon in Australia, saw a male lizard bite his female victim so hard while impregnating her that she died.

Often it is not enough to be a mere voyeur with a long lens. Like a manipulative aristocrat in a Jacobean drama, the intrepid investigator arranges things: Birkhead gets live zebra finches to mate with dead ones, Nicholas Davies and Ian Hartley make it possible for female dunnocks to take a third husband.

Decades of accumulated work of this kind have changed our understanding of the nature of sex, reproduction and the different roles of male and female. From Darwin’s time up to the late 1960s – not coincidentally, the time when the intellectual assault on male-centred academic thinking got under way in earnest – it was thought that male animals competed for female partners, with the strongest and most attractive impregnating the most females; that females sought only monogamy, and if they did have sex with multiple partners (and biologists couldn’t help noticing that they did) it was against their will, always a form of submission to rape.

In the past thirty years, the conventional wisdom has been destroyed. The truth is that females of most species actively seek multiple partners to have sex with. If the aim of males is to put their sperm into as many females as possible, females are trying, with equal determination, to get the very best sperm to fertilise their eggs – even if that means having sex with many males in turn.

Rivalry between males and discrimination by females extends beyond the sexual act itself. Inside the female, the sperm of different males fight for supremacy – this is sperm competition. At the same time, the female may be able to select the sperm that are best for her – this is sperm choice. This is the true battle of the sexes. The males and females of each species are permanently locked in a struggle to out-evolve each other as their reproductive equipment and behaviour change to achieve their conflicting aims – i.e. maximum fertilisation v. best fertilisation.

‘The very recent recognition that females of most species are promiscuous and routinely copulate with several different males, together with the realisation that in an evolutionary sense all organisms are basically selfish, has revolutionised our view of reproduction,’ Birkhead writes. ‘Sperm competition + sperm choice = sexual conflict.’

A more bizarre, extravagant or frenetic canvas of sexual behaviour than the one Birkhead paints would be hard to imagine. In seahorses, the female hands her eggs over to the male and leaves him to get on with fertilising them. To do this, one species of male seahorse ejaculates and lets his sperm rain softly down over him, fertilising the eggs.

A creature as apparently mundane as the slug goes through a baroque ordeal. Slug penises are immense – as much as seven times the length of their bodies. Far from their owners, the penises entwine and exchange sperm – and often become knotted together. The only way for the slugs to free their tangled members is for one of them to bite his off at the base. From that moment, the self-castrated slug is female-only.

Sometimes a male xylocoris, a close relative of the bedbug, will rape another male. Its sperm will make its way to the victim’s vas deferens, where sperm are stored. The next time the raped male inseminates a female, the rapist’s sperm and his own enter the female together. It is not unknown for males to be raped by other males while in the act of copulating with a female.

It isn’t always so violent or so sordid. In Australia, there’s a certain species of wren in which two-thirds of chicks are, so to speak, bastards, fathered by males outside the family group. Male wrens seeking to seduce females tout their charms by ‘plucking a yellow flower petal, which contrasts perfectly with their iridescent cobalt-blue plumage, and presenting this to the female. These displays eventually lead to extra-pair copulations when females surreptitiously slip away from home in the dim light of dawn to visit one of the males in his own territory.’

Back in the 1960s, Peter Parker was bitten by a radioactive arachnid, turned into Spiderman and acquired the ability to scuttle up the sides of tall buildings. Birkhead’s book could inspire a whole new breed of pornographic superheroes, replete with extraordinary powers and dark destinies attended by Freudian ironies. While Spiderman merely fought crime, Redback Spiderman attempts to inseminate his partner, Redback Spiderwoman, a creature a hundred times his size; if successful, he does a somersault into her mouth, and she eats him up.

In many species, it is normal for the male to offer a gift to a female if he expects to have sex with her. Sometimes this is the sperm itself. It’s nutrition of a kind. Deceitful hermaphrodite flatworms look on sex as the chance of a free lunch. In certain crickets the female snacks on a set of meaty wings specially grown by the male. But the ultimate nutritional gift a male can offer is himself. The redback spider wants to be eaten. It’s his evolutionary strategy to outfox other males and the female herself: by letting himself be consumed, he keeps her busy for twice as long as he otherwise would, making it more likely that his sperm will fertilise her eggs. To make the suicidal father more secure in his paternity, the female loses interest in sex after her meal.

The male praying mantis doesn’t mean to be killed and eaten; but a third of the time, despite their best efforts, males are foolish enough to let it happen. A successful male will stalk his mate, screening his approach with plants (and freezing if she catches sight of him), before leaping onto her back, copulating for a couple of hours, then flying away. If he mistimes his leap, his cannibalistic lover tucks in right away. Oddly enough, this doesn’t stop him having sex. Even as the female eats his head, he carries on: in fact, the loss of his head deprives him of all inhibitions and sends him into a sexual frenzy. The case of the mantis illustrates Birkhead’s point that females can be vigorous combatants in the war of the sexes. Getting himself eaten is part of the male spider’s strategy; for the mantis, on the other hand, the only winner is the female: she gets a good meal to help her produce more eggs, and is quite capable of copulating with a few more males afterwards, so the poor sacrificed man-mantis can’t even count on a posthumous fatherhood.

Reading books about the way animals have sex is liable to provoke mind-loosening transference. The comic instinct projects humanity onto the animals. The darker side of our consciousness does the reverse. A man or woman reads about the bedbug, who inseminates his partner by crashing his penis-carrier through her body like a ram-raider breaking into a supermarket, and instinctively feels a twinge of sympathetic pain in the relevant area of their anatomy. It is troubling to be reminded that human sex is only one frequency on the spectrum of animal sex; and even more troubling perhaps to think that the whole idea of love, the rock on which contemporary secular metaphysics is founded, is a sexual gimmick peculiar to our species – one at which the other animals can snigger and wonder just as we wonder at their prickly penises and hermaphrodite penetration duels.

Wary of the tendency to anthropomorphise, Birkhead steps back from the deliberately provocative title of his book when he discusses the behaviour of female animals, calling the female practice of taking multiple mates ‘polyandry’ rather than ‘promiscuity’, but like most euphemisms it ends up meaning the same thing. And Birkhead doesn’t let us forget that humans are sexual animals, too: it’s hard not to warm to a book which discusses Harold Macmillan in the context of the sexual problems of the dungfly. Paternity, in both species, is the issue: a cuckolded male who, like the former Prime Minister, spends time and energy helping to rear offspring that are not his own is letting his genes down.

It may have been the fear that his audience would make the leap from animals to humans that restricted Darwin to a false doctrine of reproduction which declared female animals to be monogamous while ignoring the signs of sperm competition which, it seems now, were staring him in the face. The prudishness of his family, haunted by the wild, un-Victorian behaviour of Charles’s grandfather Erasmus, a doctor who fathered illegitimate children and prescribed sex as a cure for hypochondria, would hardly have encouraged the great naturalist to speculate openly about motherhood, fatherhood and what might have been seen as fornication among the larger animals. Only in his more obscure works about barnacles did he permit himself to delve deeply into sexual reproduction. Dazzled by one of his discoveries, he described it to Charles Lyell:

the other day I got the curious case of a unisexual, instead of a hermaphrodite, cirripede [barnacle], in which the female had the common cirripedal character, and in two of the valves of her shell had two little pockets, in each of which she kept a little husband; I do not know of any other case where a female invariably has two husbands.

In another barnacle species he found 14 ‘little husbands’ inside a single female.

The recent acceptance of the existence of female promiscuity, sperm competition and sperm choice in animals has allowed some scientists to apply the theories to human beings with some of Darwin’s reservations. Birkhead is not one to froth at the mouth over poor science, but he doesn’t ignore transgressors either. He takes aim and blows them out of the way. This is the fate of Robin Baker and Mark Bellis, who in the early 1990s filled lecture halls and made headlines with theories applying the new doctrine to human beings. At one stage Baker told a distinguished scientific audience that men with bigger testicles would be most successful in the race to fertilise most eggs. His proof: he had asked 14 male colleagues to measure the size of their left testicles, then asked 20 female colleagues to cast their eye over the men and rank them according to whom they would most like to have an adulterous relationship with. There was a correlation between the big-balled and the sexy – but understandably, Baker’s methodology came under fierce attack.

In 1994, the work of Baker and Bellis formed the basis of a segment in the Desmond Morris TV series The Human Animal describing how men who suspected their sexual partner had recently slept with another man could unconsciously release specialised ‘killer sperm’ when they ejaculated, which went about killing the rival seed while their regular sperm concentrated on penetrating the egg. The programme even featured footage of what looked like one sperm head-butting another to death. Viewers were fascinated, but the research behind killer sperm was subsequently discredited. Birkhead, once a student and admirer of Baker, calls his work with Bellis on human sperm competition ‘little more than a sexual fantasy – phallus in wonderland’.

Are we so dull? Do the other animals get all the fun, all the baroque mechanisms of sperm warfare? After sex the male guinea pig leaves a three-centimetre plug in the female’s vagina to stop a rival male inseminating her. The sperm of the fruit fly are almost forty times its body length. Are we about as exciting as the prairie vole, whose males and females stick together through thick and thin, with occasional episodes of adultery and a certain amount of non-essential sex at the outset of the relationship to cement the bond?

Large testicles, relative to body weight, tend to be a good indicator of a species in which sperm competition is intense, and here we fare poorly against our cousins the chimpanzees. The chimp is famed for its sexual appetite, and the males have correspondingly big balls. This is not because the males inseminate lots of females. After all, if a female, once inseminated, went off to prepare for pregnancy, there wouldn’t be much need for a lot of sperm. No, the reason male chimps have such large testicles is that the females are highly promiscuous: the males are kept busy. Voracious female chimps will copulate between five hundred and a thousand times for each pregnancy, with many different males, inside and outside their own extended family group. Humans are not equipped for such marathons. Male chimps can ejaculate once an hour for five hours and still have half a tankful, whereas men tend to dry up, spermwise, if they ejaculate six times in 24 hours. Against other familiar species of mammal, we stack up badly. Our sperm is of poorer quality than other primates’, we don’t keep much in reserve, we produce the stuff at a lower rate than any other mammal yet investigated, and as for the number of sperm produced per ejaculation – we can only manage 350 million against 640 million for the rabbit and 750 billion for the boar. The only area where the human race leads is in relative penis size. As in other species, sexual conflict, the drive for control, seems to have set the human penis and vagina evolving against each other – the male always wanting to get his sperm that bit closer to its goal, the female always wanting to keep it that bit further away.

Of course, human beings sleep around, but way less than the chimp. We are also less promiscuous than many ostensibly monogamous birds. The Rev. Morris would have been better preaching to the dunnock on the virtuous ways of the human. Efforts to prove that men possess unconscious mechanisms to set sperm against sperm or that women manipulate the take-up of sperm from multiple partners have so far come to nothing. Birkhead is sceptical of surveys showing, for instance, that 4 per cent of babies born in Britain in the 1980s were the result of adulterous liaisons – although chimps, like dungflies and dunnocks, do not practise contraception. Birkhead does come up with a few intriguing stories of female human adaptive behaviour. One survey showed that as a result of long waiting lists for NHS sperm, four out of seventeen women whose husbands produced no sperm at all became pregnant before they were artificially inseminated.

Birkhead teaches behavioural ecology at Sheffield University. As he comes across here, he is one of those teachers whose lectures should be scheduled at nine in the morning to make it worth the students’ while to get out of bed. He’s witty, persuasive and clear. He knows the value of storytelling, and there are many stories here, although the book would have benefited from more of an overarching narrative to bring together the lecture-like quality of the chapters. At the outset I had the impression that sperm competition and sperm choice were now as established as male and female promiscuity. But it turns out that sperm choice is altogether more mysterious.

There is evidence that the females of certain species do have mechanisms to choose between different sperm – perhaps to select the sperm most compatible with their own DNA. Some of the signs that ‘cryptic female choice’ exists, in the comb-jelly, for instance, are persuasive. Birkhead recalls his first sight of a comb-jelly in the wild, off Coburg Island in the Canadian Arctic. ‘It was exquisitely beautiful: fist-sized, blood red and bearing row on row of iridescent cilia driving it slowly through the icy waters.’ In the book, an extraordinary series of pictures shows what happens inside the egg of this organism when it is penetrated by two sperm. The nucleus of the egg swims towards sperm number one, checks it out, appears not to like it, heads for the second sperm, likes what it finds and fuses with it to create the baby comb-jelly. Here, at the finishing line of the reproductive act, when the sperm seems to have realised its fantastically difficult aim of reaching the egg, the female has the last word.