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DID DARWIN ever think about sperm competition?

Perhaps during his barnacle period he did, when eight tedious years of dissection were enlivened by the discovery that in some species males exist as little more than bags of sperm living parasitically inside females. With each female containing two or more dwarf males, questions of paternity obviously arose. Yet Darwin made no explicit mention of sperm competition in barnacles 鈥� or any other animal.

Perhaps he didn鈥檛 appreciate the evolutionary implications of mixed paternity, but more probably he didn鈥檛 want to offend Victorian sensibilities by talking about warm-blooded vertebrate sex, either to his public or to his family. Darwin鈥檚 daughter Henrietta, who corrected the proofs of his book The Descent of Man, and Selection in Relation to Sex, also acted as his censor, slashing out anything of which she disapproved. He would never have got away with female infidelity and sperm competition.

So Darwin played safe and assumed that females were monogamous. It is only in recent years that we have come to realise how wrong he was. Promiscuity is rife among females. Instead of simply opting to mate with the best male available, many play the field and then choose whose sperm to use in the privacy of their own reproductive tracts. Exposing this cryptic female choice is proving tricky, but the hunt is starting to reveal what females are looking for in their ideal sperm.

It was Darwin himself who came up with the idea of sexual selection to explain why males and females often appear so different. Competition between males, together with female pickiness, result in greater reproductive success for some individuals. The male side of things is easy to explain: larger body size or bigger horns obviously confer a physical advantage to males vying for females. But biologists were sceptical about the female鈥檚 ability to discriminate between suitors. It was a full century before the cynics accepted that females do play an active role in choosing a mate. Even then, Darwin鈥檚 idea of monogamous females went unchallenged.

But in the late 1960s, Geoff Parker, now at the University of Liverpool, saw things that turned this thinking on its head. While watching golden coloured flies on warm dung pats, Parker noticed that the females routinely copulated with more than one male. He was the first to recognise that sexual selection does not necessarily stop once a partner is chosen, but can continue after copulation and right up to the point when sperm and egg fuse together. Males don鈥檛 compete for females, he realised, they compete for fertilisations. This breakthrough changed the way we think about sex, and Parker鈥檚 observations spawned the new field of sperm competition.

Biologists using molecular techniques to establish parentage began to realise just how common multiple matings were. DNA profiling revealed that across the animal kingdom monogamy was the exception, not the rule. In most species, the females were typically inseminated by several males during each reproductive cycle. Subsequent observation revealed that many females actually went looking for extra partners 鈥� particularly birds, which had previously been viewed as models of monogamy.

Despite all the evidence for female promiscuity, the focus remained on males. In the battle over fertilisations, females were deemed passive, reluctant and acquiescent 鈥� they just happened to be there when the action took place. This androcentric approach resulted partly from the fact that male sexual behaviour is unsubtle, vulgar and easy to record, but it also had a theoretical basis. As Parker pointed out, males have far more to win 鈥� or lose 鈥� in the competition to reproduce. Sperm competition was seen as a man鈥檚 game and the female perspective was ignored.

Then in 1996, Bill Eberhard of the University of Costa Rica published Female Control: Sexual Selection by Cryptic Female Choice, in which he championed the view that it was often in the female鈥檚 evolutionary interest to decide which of several males鈥� sperm should fertilise her eggs. He argued that by selectively using sperm from males with certain favoured traits, females could enhance their own reproductive success. And Eberhard suggested dozens of ingenious ways in which a female might do this. She could, for example, terminate copulation before a male had a chance to transfer any semen, permit insemination but later eject the sperm, retain the sperm of different males in different stores and use them selectively, or preferentially allow some sperm to travel to the site of fertilisation while holding others back.

Eberhard鈥檚 approach persuaded many behavioural biologists to think about physiology for the first time. Although much of his evidence was circumstantial, researchers were swept along by his evangelical zeal and, in a flurry of uncritical enthusiasm, they began publishing studies claiming the existence of post-copulatory female choice. Not only was there often little evidence to back up these claims, but many researchers failed to distinguish between cryptic female choice and the competition between sperm that must inevitably accompany it.

Bigger dads

One study that fell into this trap seemed to show that female yellow dung flies 鈥� the insects made famous by Parker 鈥� favour sperm from larger males. Paul Ward and colleagues at the University of Zurich, Switzerland, found that when a female dung fly copulated with two males, one small and one large, most of the offspring were fathered by the larger male, regardless of whether he had mated with the female first or second. In these experiments Ward allowed the two males to copulate for the same amount of time, ensuring, he assumed, that they each transferred a similar number of sperm. But as Leigh Simmons at the University of Western Australia, Perth, and his colleagues pointed out, larger males have larger sperm ducts. Their higher paternity rates may have had nothing to do with cryptic female choice, but could simply be a consequence of their having transferred more sperm to the female.

Even so, evidence is beginning to emerge that females do favour the sperm of certain males 鈥� though whether this is through choice or male manipulation is debatable. Martin Edvardsson and Goran Arnqvist of Ume氓 University in Sweden found that the longer a male red flour beetle spends rubbing a female with his legs during copulation, the more likely she is to use his sperm. When the researchers removed the lower part of the males鈥� legs so they could not stimulate the female, the duration of the male鈥檚 upper-leg movements had no bearing on the female鈥檚 use of sperm. Similar effects have been recorded in carrion flies. This could be one reason why many insects stroke, rub or tap females with their penises, legs or antennae while mating.

The bizarre antics of the male buffalo weaver may also fall into this category. Mark Winterbottom and I studied this starling-sized bird in Namibia, intrigued by the male鈥檚 2-centimetre-long false penis and its energetic 30-minute copulation. Sperm competition is intense because two males often share several females. During mounting the male rubs the female鈥檚 lower abdomen with his pseudo-phallus until, uniquely for a bird, he reaches orgasm and ejaculates. The aim seems to be to persuade the female to use more of his sperm than those of the other male she mates with, but so far we havn鈥檛 been able to test this idea.

Despite the difficulty of unambiguously identifying cryptic female choice, a few studies have been quite convincing. In 1996, Mats Olsson and co-workers from the University of Gothenberg, in Sweden, used DNA profiling to show that when two males inseminated female sand lizards, the male that fertilised the majority of eggs was the one genetically least similar to the female. And more recently, Ward has shown that female dung flies do indeed choose between sperm, though not on the basis of male size, but on their genes.

Nina Wilson and others at the University of Sunderland used an ingenious experiment to show that female cowpea weevils can distinguish between the sperm of different males. They allowed the same pair of males to inseminate two sets of three females 鈥� one comprised three sisters, the other three unrelated females. The researchers then looked at which male fertilised most eggs, and compared how similar the paternity was within the groups of related and unrelated females. They predicted that if there was a genetic difference between females in their preference for certain sperm, the share of each male鈥檚 paternity among the sisters should be more similar than that between the unrelated females. And this is exactly what they found.

My colleague Tom Pizzari and I have just reported in Nature a clear-cut case of females differentially using the sperm of preferred males. Female junglefowl and their free-ranging domesticated counterparts, hens, favour socially dominant males. But as males are bigger than females, subordinate males often force themselves on females. We found that hens in a free-ranging feral population frequently ejected semen immediately after insemination 鈥� and were more likely to do so following a forced mounting by a subordinate male. The female鈥檚 control of the situation is increased by the fact that ejection occurs before the male has dismounted, so he has no way of knowing whether his sperm has been retained or not.

If females are taking control over their reproductive destiny, what do they stand to gain? There was never a problem explaining why males were promiscuous 鈥� more partners meant more offspring and more copies of their genes in subsequent generations. Sometimes the benefits for females of mating with several males are also obvious. They may gain extra food, or extra help in rearing offspring. But if females just get sperm, they can benefit only indirectly, through genes passed on to their offspring. How this happens is far from clear.

The traditional, Darwinian view of female choice is that it is about females choosing superior males 鈥� with all females having a similar image in their minds about what a top-quality mate looks like. The good genes of these superior males will multiply down the generations as females choose to mate with them, thus increasing the chances that their own offspring will be desirable to the opposite sex. This theory may explain the fantastic tail plumage of the argus pheasant. And cryptic female choice could work in a similar way if a female bases her decision on the male鈥檚 appearance, status or copulatory courtship. But there is an intriguing alternative. If she decides on the basis of the attributes of the sperm alone, she must be choosing something rather different.

Jeanne Zeh of Rice University, Texas, and her husband David Zeh of the University of Houston have pioneered the idea that what females are looking for in this case is males whose genotype complements their own 鈥� compatibility rather than superiority. The Zehs propose that female promiscuity minimises the chances of females having their eggs fertilised by an incompatible male. They point out that there is abundant evidence for genetic incompatibility. Most obvious is the finding that inbreeding reduces reproductive success. And recent research shows that there are genetic conflicts within and between the nucleus and cytoplasm of sex cells. So genetic incompatibility between any two individuals may be more common than we had suspected.

Babies on show

The studies by Olsson and Wilson suggest that compatibility is at the root of cryptic female choice in sand lizards and cowpea weevils. And the Zehs, working with Scott Newcomer of the University of Houston, also have striking evidence for their idea. For several years they have studied the reproductive antics of a tiny pseudoscorpion which inhabits rotting wood in Central American forests. This arthropod is unusual in several ways, not least its habit of moving from stump to stump by riding on giant harlequin beetles. It also has a revealing mode of reproduction. The female pseudoscorpion deposits her eggs into a translucent external brood pouch, allowing researchers to monitor the survival and hatching of the developing babies 鈥� something that is impossible in other animals that produce live young.

What Newcomer and the Zehs found was that monogamous females 鈥� those inseminated by only a single male 鈥� aborted significantly more of their developing embryos than females that copulated with two males. Each female had received the same amount of sperm, so the effect had to be a result of sperm quality rather than quantity. The researchers concluded that the abortions occurred because of genetic incompatibility between certain partners and that multiple matings are a pre-emptive strategy to avoid this kind of reproductive failure. In pseudoscorpion society, promiscuous females are more successful.

Another bizarre observation could also be the result of a female鈥檚 search for a compatible mate. The eggs of the comb jelly are transparent, providing researchers with a window on the process of fertilisation. When Danielle Carr茅 and Christian Sardet of the Zoology Station at the Oceanography Institute in Villefranche-sur-Mer in France, looked through it they saw something remarkable. The eggs were typically penetrated by several sperm, whose nuclei each form a male 鈥減ronucleus鈥� inside the egg鈥檚 cytoplasm. The female genetic material 鈥� the female pronucleus 鈥� then moves through the cytoplasm visiting each male pronucleus in turn, before going back to fuse with one of them. The researchers describe this as being just like mate choice, but happening at the nuclear level.

Are the female pronuclei of comb jellies searching for a compatible other half? As yet, the evolutionary benefits of this strange behaviour remain a mystery. What is clear, however, is that comb jellies are playing the same game as many other animals. While males are continuously evolving ways to outwit each other in sperm competition, females have a chance to take advantage of the situation. So we should not be surprised to find that, for some females at least, promiscuity is the road to success.