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Darwin may have discovered sexual selection – the theory that some individuals are inherently more successful at choosing or competing for mates than others – but he was touchingly naive about sex. He seems to have assumed, for instance, that most female animals are strictly monogamous for life. Today, long freed from the social mores that constrained Victorian thinking, research into the behavioural and physiological mechanisms that sustain sexual selection is booming – and proving beyond doubt that nothing could be further from the truth.

One of the most fruitful areas of research revolves around the problem of ‘sperm competition’. When females behave promiscuously, copulating with more than one male in a single reproductive cycle, to what extent do they and their various partners contrive and compete to influence the outcome? Over the past few years behavioural ecologists have begun to trawl for clues in an unlikely quarter: genetic fingerprints of birds.

The problem of sperm competition scarcely occurred to Darwin and his immediate successors. In the decades following his death, biologists clung to the notion of female monogamy in certain species. Even when they saw supposedly monogamous females acting promiscuously, they would dismiss the behaviour as due to sickness or hormonal imbalance. Only in the 1970s, when biologists began to try to understand animal behaviour in terms of the overriding urge to pass on genes, did the meaning and complexity of promiscuity in animals begin to emerge.

Farewell to monogamy

One of the pioneers of change was Geoff Parker of the University of Liverpool. Indeed it was Parker who in 1970 coined the term ‘sperm competition’, which biologists now use to describe all the behaviours and physiological responses, of males as well as females, associated with promiscuity. Immediately following Parker’s lead, most researchers studied sperm competition among insects. Birds were considered unpromising subjects because a well-known survey of the world’s birds, published in 1968, had claimed more than 90 per cent of species were monogamous. But during the next decade or so researchers accumulated an enormous body of data on the sexual behaviour of birds, and belief in strict avian monogamy began to crumble.

The first attempts to study the kinds of behaviour underlying sperm competition in birds focused on males. This is not surprising, for in many species, it is the males who are the most conspicuously eager for ‘extra-pair’ sex. Take the common guillemot (Uria aalgae). Like virtually all sea birds, the guillemot is monogamous, at least in the sense that both partners must work together to rear a chick. Its pairings, moreover, are for life. Even so, the bird breeds in the avian equivalent of tenement blocks – large, closely-knit colonies – and males in particular are quick to exploit the situation.

For instance, if a male guillemot is slow off the mark when his partner solicits copulation – which she does by falling forward into a prone position and uttering a distinctive call – other males will leap onto her. The female guillemot invariably resists insemination but is sometimes overcome. Some males will even attempt to squeeze themselves between a bonded pair while they are copulating, subtlety not being part of their make-up. The males of many other bird species, including the white-fronted bee-eater (Merops bullockoides), mallard duck (Anas platyrhynchos) sand martin (Riparia riparia) and indigo bunting (Passerina cyanea), behave just as opportunistically.

For years, behavioural ecologists – or at least the males among them – interpreted this combination of male rapacity and female resistance as a sign that only the male birds stood to gain from the liaison. One way a female might lose out from adultery, they reasoned, would be if her partner, suspecting he had been cuckolded, withdrew his parental support once the chicks had hatched. Today we know better. After more careful research – and the occasional verbal battering from female colleagues – most behavioural ecologists have come to realise that such notions were founded on the blinkered observations of male chauvinists. In reality many female birds actually seek adulterous copulations. Far from being passive victims of adultery, they are active and willing participants.

A turning point in the field of sperm competition came in 1985 when Alec Jeffreys at the University of Leicester discovered that each human being has a unique set of DNA fragments which are detectable as genetic ‘fingerprints’. Quick to realise the technique’s potential for studying animal sexual behaviour, Terry Burke at the University of Leicester and David Parkin at the University of Nottingham began to apply DNA fingerprinting to birds, using it to check both paternal and maternal parentage of offspring.

Seven years on, DNA studies of parentage are now routine if still somewhat slow (it can take several weeks to produce a genetic fingerprint). Birds are particularly convenient subjects because, unlike mammals, their red blood cells have nucei, so only a tiny drop of blood is needed to produce the DNA fingerprint. But they are not the only suitable subjects. ¿ìè¶ÌÊÓƵs studying the genetic basis of human disease, for instance, regularly take DNA fingerprints of their subjects in order to double-check their parentage.

High-rise infidelity

Unlike the bird studies, however, research on human parentage is seldom, if ever, published in any detail. Mainly this is to preserve anonymity – crucial when the subjects do not know their parentage is to be checked as part of the study. Privately, though, most medical geneticists say that about 10 per cent of their subjects are sired by men other than their avowed fathers. One study, however, allegedly of the inhabitants of a high-rise apartment block, has claimed a much higher figure – 30 per cent.

But whatever the scale of human adultery, it is dwarfed by that of some bird species. The Australian splendid fairy wren (Malurus splendens) is a case in point. The bird breeds communally, in groups that usually comprise one male and female pair and several male helpers, who all work together to rear a brood. A DNA study, by Ian Rowley, formerly of the CSIRO (the Australian national research organisation), and his colleagues, reveals that 65 per cent of the offspring are, on average, fathered by males outside this small communal group.

Adultery is rife even in species that breed in conventional pairs, such as the pied flycatcher (Ficedula hypoleuca), blue tit (Parus caeruleus), indigo bunting and white crowned sparrow (Zonotrichia luecophrus). David Westneat of Kentucky University, for example, has found that almost half of all indigo bunting broods contain offspring fathered by roving males, amounting to about one-third of all chicks. Yet in some species (notably the fulmar petrel, Fulmarus glacialis) adulterous copulations, though they certainly take place, produce no offspring.

What is the origin of this variation? Part of the answer must lie with how effective male partners are at safeguarding their paternity . But equally important are the extent to which female birds seek adulterous copulations and the relative effectiveness of these copulations in producing offspring.

If adulterous copulations are just as effective as copulations between partners, then the proportion of offspring fathered by roving males – as determined by genetic fingerprinting – should be roughly the same as the proportion of adulterous copulations observed in behavioural studies. For many species, this correlation is exactly what is seen (see Figure 1). But in some, the number of ‘extra-pair’ offspring is disportionately large. Why should sex with a stranger be any more successful than copulating with a life-long partner?

A simple explanation is that such observations are not to be trusted. Adulterous copulations may be difficult to count accurately, particularly if the couples are unusually discreet. But a more intriguing possibility is that they are genuinely more potent – that is, involve the transfer of more sperm to the female – than copulations between partners. One of us (TB) is working with Bobbie Fletcher at the University of Sheffield to test this theory in research on the sexual behaviour of the Australian zebra finch (Taeniopygia guttata).FIG-mg18284802.GIF

Adultery is common among zebra finches. But as with most bird species, the male desists during the week-long periods when he is copulating with his partner. As soon she is no longer fertile and safely incubating the eggs, however, the male wastes no time in seeking out other females. So the first question to ask is, does the timing of the male’s search affect his sexual potency? To answer this, we allowed captive male zebra finches to copulate with other females, both during and after periods of copulation with their mates. Immediately after each copulation, we collected sperm from the females without harming them.

Sperm or spare?

The result was clear-cut: as soon as the period of copulation with their partners ended, the males transferred more than twice as many sperm to the other females. But interpreting this observation was trickier. Did the male zebra finches simply have fewer sperm to spare for other females when they were copulating with their mates? Or did they control the number of sperm they transferred? Unfortunately, this issue is still unresolved, as is the broader question of whether any male animals can control the number of sperm they transfer during copulation. Over the past year or so the debate has been stirred by a controversial series of studies – on humans, rats and insects – which indicate that males do have this ability .

So much for the male’s role in sperm competition, what of the female’s? Traditional definitions of mating systems tend to reflect social rather than sexual relationships. Whether we call a species polygynous (one male with many female mates), polyandrous (one female with several male mates) or monogamous (one male and one female working together to rear one or more broods, remaining sexually faithful throughout) invariably depends on what we know of the animals’ social behaviour – not its sexual behaviour.

Yet, as the parentage studies of birds so powerfully reveal, females are quite capable of being socially monogamous but sexually polyandrous. And herein lies a puzzle. Why should a female bird go to the trouble of pairing up with one male, only to go looking for others? What does the female gain by adultery?

In other animal groups, such as insects, females sometimes gain material benefits like food from copulating with several different males. But this doesn’t appear to be the case with birds. Nor do the females of socially monogamous bird species receive any help from roving males in raising broods. The only possible gain for the female appears to be in improving the genetic make-ups of her offspring.

Female birds that copulate with several males are likely to produce genetically diverse broods, which in an unpredictable environment may improve their prospects. But this cannot be the whole story, for even females who mate with same partner will produce offspring with varied genetic make-ups. A more important factor may be the desire to procure good quality genes.

In theory, copulating with males who are genetically superior to their mates could benefit females in two ways. They may produce ‘sexy sons’ – male offspring who are more attractive to females, and so more likely to produce equally irresistible sons – or they may produce a brood which is generally more vigorous or resistant to parasites and other pathogens. Biologists have striven hard to design experiments to test this theory. Despite their efforts, however, there is still no consensus over whether either of these benefits lies at the root of female adultery. Moreover, if female birds do choose to copulate with ‘superior’ males, why should they bother to pair up with second-rate males in the first place? Once again, there is no consensus among biologists, but we believe that in some cases the birds have no choice.

With migratory species such as the barn swallow (Hirundo rustica), males arrive at the breeding grounds a few days ahead of the females. The first females to arrive, therefore, will have the pick of all the available males; the fashionably late will have rather less choice; while the stragglers will be forced to take males with relatively poor genes if they wish to breed at all (a partner with poor genes is better than no partner because he will at least help in rearing the brood). It is these late arrivals who would stand to gain most from adulterous liaisons with ‘good quality’ males.

The main assumption here is that female birds are inherently choosy about their partners and don’t simply pick them at random. Evidence that they are comes from the breeding behaviour of ‘lekking’ species such as the sage grouse (Centrocercus urophasianus) and black grouse (Tetrao tetrix) and South American cotingas. Leks are breeding sites where avian courtship rituals take place: males display, and females, visiting for the sole purpose of copulation, make their choice.

Nothing but the best

The females select one male each, mate once, store the sperm and then leave the lek. Later they use the sperm to fertilise their eggs and subsequently rear the offspring alone. The most important point is that, although each female copulates only once, they generally agree about which male is the ‘best’. Typically one, or at most a few, males on the lek will receive the bulk of the attention.

Choice of mate, then, is vital to the females of lekking species. Is it also vital for the females of socially monogamous and polygynous species? There is increasing evidence that the females of many such species – the swallow (Hirundo rustica), blue tit, black-capped chickadee (Parus atricapillas), bobolink (Dolichonyx oryzivorous) and zebra finch (Taeniopygia guttata) – do indeed choose good quality males for adulterous liaisons.

One clear sign of choice in some species is that young females with young mates copulate with other males more frequently than older females and those paired to older males. A remarkable example of this kind of behaviour was reported in 1990 by Eugene Morton of the Smithsonian Institution in Washington DC.

Studying the North American purple martin Progne subis, Morton found that, typically, one old male will monopolise a group of nest sites, pair with one female and then, after she is no longer fertile, actively encourage young males to use the remaining nest sites. These young males then attract females, who pair with them. Surprisingly, however, these females also copulate with the old male, who ultimately fathers about 70 per cent of their offspring. Longevity, it seems, may be a sign of good genes.

The idea that socially monogamous female birds use adultery to improve the genetic lot of their offspring may explain why female guillemots resist enforced insemination. What would they gain from copulating with a male whose genes are no better than their partners’? What is less clear, however, is whether a female who copulates with a stranger stands to lose the support of her partner in rearing the brood. So far only one report, a 1990 study of dunnocks, has found this to be the case.

For birds that form some kind of social bond, female choice in adultery is only part of a many-tiered process of mate selection. The females of many species can choose to break a pair bond and find another partner. They can also select the time of copulation, which is sure to be crucial in determining who sires their offspring: in all birds studied to date, the last male to inseminate a female before she lays her eggs fathers the majority of offspring.

Dangerous journey

Yet timing is not the only way a female bird may influence the success of sperm. The female reproductive tract is notoriously hostile to sperm and only a tiny proportion of the sperm inseminated ever get anywhere near the female’s eggs. ¿ìè¶ÌÊÓƵs are still locked in debate over precisely why so many sperm die en route. There is certainly a physical hurdle to overcome – a long and circuitous tract – but inceasingly researchers believe that many sperm fall foul of specific immune responses mounted in the tract following insemination.

Biologists have come up with three explanations as to why the female reproductive tract evolved in this extraordinary way. One idea is that it did so to control bacteria and pathogens, a warlike operation that leaves massive numbers of journeying sperm caught in the crossfire. Another is that hostility helps to reduce sperm numbers and hence avoid polyspermy (the penetration of eggs by more than one sperm) which invariably results in embryo death. But the third, and to our minds most fascinating, possibility is that it helps to prevent eggs from being fertilised by unfit sperm – to separate the wheat from the chaff, as it were.

The study of sperm competition in birds has come a long way in just a few years. The future of the discipline promises to be even more exciting, as more and more studies based on DNA fingerprinting are completed. A key result has been how widespread sperm competition is, not just among birds but throughout all animal species, and how far-reaching are its effects on their lives. Moreover, because the subject deals with the physical – counting sperm, measuring sperm storage tissue and so on – behavioural ecologists are being forced to think about underlying mechanisms and physiological constraints on behaviour, as well as how that behaviour helped the animal to adapt.

Journal reference: Sperm competition in birds: Evolutionary Causes and Consequences by TR Birkhead & AP Moller, Academic Press, 1992.