'So many men, so little time'

That's what Mae West reckoned. But are women really pre-programmed to be promiscuous? Not if the size of men's testicles is anything to go by. Tim Birkhead explains why
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The Independent Online

Female birds do it, female honey bees do it; female mites, crabs, fish, reptiles, even female mammals are at it. They all copulate with several different males each breeding cycle. Biologists are used to the concept of male promiscuity, but promiscuous females are a whole new ball game. Until recently, scientists thought promiscuity was not in the interests of females but a number of studies over the past few years clearly show that having sex with many different partners can no longer be seen as an exclusively male preserve.

Female promiscuity generates a special form of competition between males - competition between their sperm for fertilisations. Charles Darwin, and until about 1970 most of his followers, assumed that competition between males and the act of choosing between male suitors by females - processes which together comprised his ingenious idea of sexual selection - ceased at mate acquisition. The recent discovery of female promiscuity means that sexual selection continues after copulation.

In the currency of evolution, males do not compete for females, they compete for fertilisations. By doing so, they generate what is referred to as sperm competition. The more likely it is that females copulate with different males, or the more males they copulate with, the greater the intensity of competition between sperm in the female's reproductive system.

Let's consider birds. Like us, in most species a male and female rear babies together as an apparently monogamous pair. Yet DNA studies reveal that often the babies a male helps to raise are not his own. In the reed bunting, 55 per cent of all offspring are fathered by other males. In swallows it is 25 per cent, in blue tits and house sparrows the figure is 12 per cent. True sexual monogamy is a rare thing: Shakespeare's model of avian monogamy, the swan, is one of the few birds to have remained unsullied by the molecular revolution.

The evolutionary benefits to males of such promiscuity are obvious: more offspring and more copies of their genes in subsequent generations. But until the mid-1980s it was assumed that females gained little or nothing from being promiscuous. The naive view that females were passive, acquiescent participants in infidelity was shattered when the females of some birds were seen actively seeking illicit matings.

What about humans? Researchers have used three techniques to try and discover the extent to which female promiscuity occurs: questionnaires, paternity studies and anatomical evidence.

In their 1995 book, Human Sperm Competition (London: Chapman & Hall), biologists Robin Baker and Mark Bellis suggest that females in contemporary Western society are rather promiscuous. Based on their questionnaire in Company magazine, they estimated that between 4 and 12 per cent of all copulations are what they called "double matings"; that is, women had copulated with two different men within five days, thereby providing the opportunity for sperm competition.

Their review of paternity studies also suggested frequent infidelity, with extra-pair paternity running between 1.4 per cent and 30 per cent in different communities. Finally, Baker and Bellis presented some extraordinary anatomical information to support their promiscuous standpoint. As anyone who has worked in a fertility clinic knows, the variation in the shape and size of spermatozoa in human ejaculates is incredible. The conventional wisdom was that sperm are difficult to make and variation in sperm morphology represented production errors. In a remarkable bit of lateral thinking, Baker and Bellis turned this on its head and proposed that instead of being mistakes, different sperm types had evolved specifically in response to sperm competition generated by female promiscuity.

Their most extreme idea was "kamikaze sperm" - sperm which, on contacting those of another male, exploded and killed both themselves and their rival. Although this might sound surreal, similar things have been recorded in other animals. Baker and Bellis's evidence for intense sperm competition in humans was ingenious and very sexy, but unfortunately it has not survived subsequent scientific scrutiny.

Their survey achieved a less than 1 per cent response from Company magazine's 439,000 readers. Moreover, the readers of Company magazine were unlikely to constitute a random cross-section of British females. Much larger, more reliable surveys conducted later in the UK, America and France as part of Aids research revealed much lower levels of female promiscuity than Baker and Bellis reported.

One might have assumed that Baker & Bellis would have been on firmer ground with the results from paternity studies, but they were not. First, genetic mismatches between putative parents and offspring can occur for several reasons other than extra-marital matings, including mate-switching, adoption, and possibly even the occasional mix up of babies on the maternity ward. The most detailed published information on paternity comes, not as you might expect from the new sophisticated DNA analyses, but from blood-group studies. These are notoriously imprecise because they can say only who is not a particular child's father. The bottom line is that we do not really have a good feel for the current level of extra-pair paternity - a measure of female promiscuity - in humans.

As far as killer sperm are concerned, they died a death when Professor Harry Moore and colleagues at Sheffield University repeated Baker and Bellis's key experiment using more sophisticated methods and couldn't replicate the previous results. This is not to say that sperm competition and female promiscuity are absent in humans - obviously they are not. But these results suggest that sperm competition might not be as important as Baker and Bellis presumed.

The best evidence that humans evolved with only a degree of sperm competition comes from some additional anatomical studies. Across a range of different non-human animals, males are found to have relatively larger testicles in species with more intense sperm competition. This makes sense - males can swamp the competition by inseminating more sperm, and bigger testicles produce more sperm.

This association between relative testicle size and the intensity of sperm competition is so consistent that we can use it to gauge the basic level of sperm competition in humans. Among gorillas, for instance, female promiscuity and sperm competition are almost unknown: the male's testicles are relatively tiny, weighing in at a mere 30g or 0.03 per cent of body weight. Chimpanzees, on the other hand are highly promiscuous (females may copulate a thousand times for each pregnancy), and despite their smaller body size males have huge testicles - 119g or 0.3 per cent of their body weight. Human testicles fall in between these two simian extremes (40g or 0.08 per cent of body weight), suggesting only modest levels of female promiscuity in our evolutionary past.

Other anatomical evidence pushes us even further into the monogamy zone: compared with most other mammals our reproductive potential is pathetic: human testicles produce sperm only slowly and our reserves are an embarrassment: six ejaculations in a day and men are a spent force (a chimpanzee can go on for another six).

Even if humans have a naturally low level of female promiscuity, it requires an explanation. One possible benefit females might gain from promiscuity is more care for their offspring. A study of a small brown bird, the dunnock, by Nicholas Davies at Cambridge University, showed that females that copulated with two males got more paternal care and as a result reared more offspring compared to females in monogamous relationships.

That the same might be true in some human societies is dramatically demonstrated by the Ache, a group of South American indians whose first contact with white anthropologists occurred as recently as 1972. Kim Hill and Magdelena Hurtado of the University of New Mexico established that life before Westerners in this pre-literate society was ferocious and brutal. Inter-tribal warfare was common and even within their own groups status-driven club fights resulted in high male mortality.

Infants without fathers fared badly. A fatherless child had a mere 50 per cent chance of survival, compared with 86 per cent for those with a father present. To increase their chances of passing on their genes, females had taken matters into their own hands, and routinely copulated with several males, thereby confusing paternity. With no real marriage as such, females ensured this way that there was always at least one male who thought he might be the father of a particular child, and hence provided care for it. It actually paid to be promiscuous for females in this human society.

Tim Birkhead is the curator of the Alfred Denny Museum at the University of Sheffield. His book, 'Promiscuity', is published this week by Faber & Faber, £9.99