Sex and sensibility

July 2000, a bird journal known as The Auk published a photograph of the little-known Argentine lake duck Oxyura vittata, sending shock waves through the ornithological world. So striking was the image that a year later Nature reproduced it, to the amazement and amusement of its readers. The image was of the duck's startlingly long phallus - almost as long as the bird's body and relatively longer than in any other bird or mammal.

Ducks are one of a handful of birds that possess a penis (the rest make do without), but this was truly exceptional. They are socially monogamous, but males are sexually promiscuous and always looking for extra-curricular mating opportunities, regardless of whether females are interested or not. Biologists assume that a penis facilitates the duck's unpleasant habit of forcibly mating with other males' partners.

What would Charles Darwin have made of the Argentine lake duck's extraordinary appendage? I think he would have been more intrigued than shocked. After all, when writing an account of the barnacles he spent eight years dissecting, he gleefully described the penis of one particular species as "wonderfully developed ... when fully extended, it must equal between eight and nine times the entire length of the animal", lying "coiled up, like a great worm".

In his two barnacle volumes published in 1851 and 1854, Darwin was uncharacteristically frank about matters sexual because - it is said - he thought that no one other than scientists would read them. Later, with an increasingly public profile, he became noticeably more cautious.

Eight tedious years of dissecting barnacles paid off. They made Darwin the world expert on the subject and gave him scientific credibility. The tedium of this protracted zoological apprenticeship was broken by his discovery that some barnacles had separate sexes (most were hermaphrodites), and by finding one species in which males lived as tiny parasites inside the female's body.

Excited (who wouldn't be?), Darwin wrote to his friend and mentor, geologist Charles Lyell, to tell him that in one particular species the two halves of the female's 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".

Describing these dwarf males as little more than bags of spermatozoa, Darwin discovered other barnacles with as many as 14 miniature males and speculated that any one of them might fertilise the female's eggs.

We now know that the females of a number of animal species typically have two or more husbands. The commonest example may even be in your garden as I write - the dunnock, more widely known as the hedge sparrow. Unstudied for years, it was discovered in the 1970s that female dunnocks typically form a polyandrous relationship with two males. A similar system operates in those tiny primates known as tamarins.

Other birds with a polyandrous mating system include the tropical jacana or lily-trotter, and studies by my doctoral students showed that the buffalo weaver of Africa and the vasa parrot of Madagascar were polyandrous too, the vasa parrot being extraordinary in mating with at least eight different males.

Multiple male partners can create a certain tension in a relationship and this is no less true in dunnocks, weavers or vasa parrots than in humans, for natural selection will favour the male that successfully fertilises the female's eggs. In a polyandrous relationship males compete for fertilisations, and sperm competition is inevitable.

Sperm competition isn't confined to animals with a stable polyandrous mating system. We now know that despite most birds, including tits, sparrows and starlings, having a socially monogamous mating system, extra-pair matings and fertilisations are common because females are promiscuous. What's more, this seems to be true across the entire animal kingdom, with genuine female sexual monogamy being as scarce as hen's teeth. (In case you are wondering, seahorses and mute swans seem to be completely faithful.)

Darwin came within a whisker of recognising the significance of female promiscuity and sperm competition. After completing his study of barnacles he moved on to something much more interesting - pigeons, birds famous for their fidelity.

But Darwin, who was obviously a sharp observer, nonetheless noticed that extra-pair liaisons still occurred, writing that "when a male does break his marriage-vow, he does not permanently desert his mate". Notice here that it is the male rather than the female breaking the vows - did Darwin not recognise that it takes two to perform an Argentine tango?

Even more remarkable was Darwin's account of infidelity among his cousin's geese. William Darwin Fox, Darwin's university buddy, became a rector and kept a menagerie, from time to time sending zoological titbits to his more scholarly relative. One of these concerned Fox's geese, of which he had two sorts: common white farmyard and brown Chinese geese.

The two types had lived amicably separate lives until one year a Chinese gander seduced a female common goose. When this female's brood emerged it was apparent that there were two fathers, with the Chinese gander responsible for most of the offspring. It would be hard to have a clearer demonstration of infidelity, sperm competition and multiple paternity, yet for some reason Darwin chose not to comment.

If Darwin had put two and two together, the study of sperm competition - now a major area of research - might have been launched in 1870 rather than 1970. Why did Darwin ignore the evidence and why did it take a century for others to make the connection?

I have spent several years asking myself this question, searching for an answer among Darwin's voluminous but intriguing correspondence, as collected by the Darwin Correspondence Project (http://www.darwinproject.ac.uk/).

There are several possibilities, one being that Darwin was a prude. Certainly in Victorian times it was not the done thing for a figure such as Darwin to discuss his ideas about female promiscuity in public. It was fine to write about the sexuality of plants, but Victorian mores meant that animal sex was out of bounds - at least in Darwin's writings intended for public consumption.

Then there was family embarrassment. Darwin's grandfather, the polymath and physician Erasmus Darwin, had been a libertine and fathered illegitimate children.

A sexual enthusiast, grandad Darwin wrote enormously long poems about the sexual parts of plants and gaily prescribed sex for his female hypochondriac patients. However, just as Darwin was writing his book on sexual selection in the late 1860s, the discovery of yet another of grandad's illegitimate descendants must have dampened his own enthusiasm for sex, or at least writing about it.

If Darwin was a prude, he wasn't as prudish as his publisher, John Murray. Darwin had decided to call his book on sexual selection The Descent of Man and Selection in Relation to Sex. Murray pleaded with him to remove the S-word from the title, but Darwin stuck to his guns. As far we know, few noticed and even fewer seemed to care.

Perhaps the single most important influence on Darwin's writing about sex was his daughter Henrietta, or Etty as she was known. When Darwin was writing Descent Etty was in her late twenties, still living at home and not yet married (she married in 1871, the year the book was published). She helped her father to correct the proofs of Descent, but also acted as his censor. This was apparent when Darwin wrote a short biography of Erasmus Darwin, only for Etty to slash her red crayon through Darwin's reference to grandad's "ardent love of women".

Potentially far more offensive to Victorian ladies were Darwin's comments on monkeys' "bottoms". Fascinated by these colourful swellings and their role in sexual selection, Darwin knew that they were not the female monkey's bottom but her greatly enlarged genitalia. In an effort to avoid offence, Darwin wrote this section of Descent in Latin, which Etty at least was unable to read. Others, however, could - and some, such as the artist and social commentator John Ruskin, were offended.

When Emma Darwin took her husband off to the Lake District for a holiday in 1879 they were invited to Ruskin's home for lunch. Sixty years old and at the peak of his fame, Ruskin considered Darwin's evolutionary ideas to be "pernicious nonsense". After their visit Ruskin sent the Darwins a message saying that Charles would be better employed "bottling air" than contemplating the "hinder parts of monkeys". Darwin wrote back, saying good-naturedly that he was impressed that Ruskin even knew of his "deep and tender interest in the brightly coloured hinder half of certain monkeys".

What Darwin probably didn't know was that Ruskin had a thing about primate nether regions, and there is a story that Ruskin failed to consummate his marriage to the delightful Euphemia (Effie) Gray because of his discovery on their wedding night that she had pubic hair. In reality, it was probably her periods that put him off. She remained a virgin and later left Ruskin to marry his protege, the Pre-Raphaelite painter John Everett Millais.

In these liberal times it is hard to imagine what it must have been like living in sexually repressed Victorian England. We can glean a sense of it, however, from Etty Darwin herself. In later life she single-handedly began a campaign to have the stinkhorn fungus - whose Latin name, Phallus impudicus, simultaneously both identifies and describes it - removed from the English countryside because of its influence on the maids.

Now if you or I were to undertake such a campaign, we would simply squish the stinkhorns underfoot - a tad messy perhaps, because they are rather gelatinous, but by far the easiest way to destroy them. But Etty didn't do that. Instead, she picked them, brought them home in a napkin-covered basket and burnt them in the privacy of her study. Hmmm.

The upshot of all this was that Darwin steered clear of female promiscuity and plumped for female monogamy, an idea that then remained firmly fixed, in biologists' minds at least, for a full century. The significance of female promiscuity only really became apparent in the early 1970s with the realisation that natural selection operated on individuals rather than groups or populations.

Biologists take this for granted today, but 40 years ago most scientists in the field had only a muddy concept of what Darwin meant or said. Anyway, renewed focus on the individual made it apparent that males and females might have different evolutionary agendas.

Rather than reproduction being a joint venture with mutual benefits, it was suddenly appropriate to ask who benefited - males or females? For males, it was intuitively obvious that more partners meant more offspring, which meant more genes handed down to subsequent generations. The issue for females was more subtle.

For a long time it was unclear how females could benefit from being unfaithful. Unlike males, who can potentially father dozens or even hundreds of offspring, the females of most species are limited in their reproductive output, so promiscuity is unlikely to increase the number of offspring they produce. Eventually, it was realised that by the careful choice of extra-pair partners, a female might increase the quality of her offspring, and studies of several different animals have since confirmed this.

I don't think Darwin thought this subject through. I don't think he ever thought carefully enough about the reproductive consequences of individual selection. As far as I can see, there isn't a hint of this kind of thinking in his voluminous correspondence. This is curious because the idea of female choice was such an integral (albeit controversial) component of his concept of sexual selection. For Darwin, mate choice simply stopped at copulation.

Although Darwin clearly missed a trick here, he was always receptive to new ideas and excited by novel observations. I like to think he would have been delighted by one very recent discovery concerning the sex lives of ducks.

To counter unwanted attention from males and their enormous phalluses, female ducks appear to have evolved the most anatomically elaborate vaginas of any bird species, with blind-ending ducts and a curious corkscrew spiral - all designed, as far as we can tell, to keep the male at arm's length, so to speak, and to avoid extra-pair fertilisation. Darwin would have loved it.

BIOLOGY'S GRAMMARIAN: DARWIN'S DANGEROUS IDEA TODAY

This year we celebrate the bicentenary of Charles Darwin's birth and the 150th anniversary of his seminal work, On the Origin of Species by Means of Natural Selection. Here, academics from science and religion discuss what his theories mean today

Janet Smith is lecturer in biosciences, University of Birmingham

There is no doubt that the work of Darwin is still highly relevant to the modern-day scientist. His influence still permeates the way in which we do science today. Nowhere is this influence greater than in contemporary bioscience or in a biomedical research laboratory such as mine.

Darwin's work is important and still relevant to my work and teaching as a geneticist and developmental biologist. Darwin's theory of mutability, which we now know acts at the DNA level via gene mutation, and his foresight in listing problems with it, many of which have now been resolved, are essential.

Darwin was not the father of biology, just as Newton was not the father of physics. But like all influential scientists he was flexible of mind, hard-working, insightful and lucky enough to have the resources he needed to generate the data required to support and refine his big idea.

His insightful hypothesis, the "unifying theory" of speciation described in On the Origin of Species, is fundamental to how we understand and interpret scientific data today - not least for the sheer volume and all-encompassing nature of experimental work and data that Darwin produced to support his premise.

His approach, in which hypothesis and real data combined to generate a novel and lasting paradigm shift in our understanding of ourselves and the natural world, is a model for the scientific method and evidence-based research today.

John McCarthy is director of the Manchester Interdisciplinary Biocentre, University of Manchester

Darwin's ideas on evolution driven by natural selection represent one of the most important milestones in the history of science. It is easy to forget today, 150 years after their first publication, just how dramatic a change in humanity's perception of living organisms (including itself) was brought about by these revolutionary ideas.

Indeed, possibly more than any other scientific theory, the concept of what we now call "Darwinian selection" has exerted a pervasive effect on both science and human culture.

Had he been alive today, Darwin would have been fascinated by the progressive elucidation over the past 50 years of many of the molecular principles that underpin evolutionary changes.

He would also have been impressed by the increasing role of methods and concepts from the physical sciences and engineering in revealing how complex interactive networks of molecules in biological systems generate the emergent properties that we recognise as "living".

But probably he would have been most excited to learn that the knowledge of naturally evolved living systems acquired over the past 150 years now allows us to design and engineer at least sub-cellular synthetic systems that are effectively selected in silico.

By identifying the interplay between physical forces (rather than divine intervention) and biological adaptation, Darwin helped initiate a chain of events that has radically changed our world.

Gavin D'Costa is professor in Catholic theology, University of Bristol

Darwin was misunderstood by many Christians, so much so that the Anglican Church has issued an "apology" to mark Darwin's bicentenary and the anniversary of On the Origin of Species, rather like the Roman Catholic Church's apology to Galileo. So what is at stake? Three things.

First, that Christians engage intelligently over scientific debate with the quiet confidence that there cannot be a contradiction regarding the truth of God and the truth of science.

Second, this a priori starting point means that if the latter throws up a well-established finding over hundreds of years, then theology needs to rethink whether it has trespassed over its legitimate boundaries if it finds itself contradicted.

Third, if theology is confident of its truth and there is still a contradiction, science must be subject to rigorous scrutiny, especially its presuppositions and context.

Darwin's followers have sometimes developed his theses into theories that are in direct opposition to theological claims and this debate remains unresolved.

So let's celebrate this pioneer, never be afraid of truth and continue this important discussion.

Gerard Loughlin is professor of theology and religion, Durham University

Darwin gave us back a more ancient way of thinking about our place in nature. For example, the Roman poet Ovid had imagined a world in which all things change, in which no forms are stable and everything can become something else.

Darwin endowed this metamorphosis with the regularity of law and mechanism and an almost endless duration: a taming but also an expansion of the mercurial imagination.

But it was Darwin's misfortune to have encountered a modernised Christianity, one obsessed with the security of the unequivocal and forgetful of a time when its holy scriptures were poetic as well as historical, teaching truly with figures of speech.

Medieval Christians were as disturbed by mutability as anyone today, but they did not think it was impossible.

Indeed, they saw it all around them and honoured it in the transmutation of the sacraments. They hoped that they themselves would be changed in the twinkling of an eye. In this they were more Darwinian than many of their modern counterparts.

Darwin lacked the theological resources to marry providence with contingency, to remind him that God gave as much thought to the sparrow or the dinosaur as He to Himself.

Darwin teaches that we do not transcend nature - faith invokes what does.

Steve Jones is professor of genetics, University College London

Darwin, to me, was the man who invented biology. Before On the Origin of Species there were plenty of excellent scientists out there working on fossils, animal breeding, the insects of remote lands, the behaviour of birds and much more.

None, though, realised that they were all doing the same thing: studying aspects of evolution. The famous book's "long argument" made that clear (even if the word "evolution" does not appear in it).

We seem to have forgotten just how radical the notion must have seemed when it first appeared. Now, it is common - even commonplace - to see information from distantly related creatures, neurobiology and DNA sequences in the same scientific paper.

So used are the people at the bench to Darwin's great idea that they sometimes forget how important it is. It's a bit like a language; everyone uses grammatical rules without realising it and only when learning a new one does the importance of formal rules emerge.

Darwin gave biology a grammar - the theory of evolution. To become an expert in the subject you have to start there first.