原文地址 http://www.newscientist.com/article/mg21028171.800-sex-and-asymmetry-how-the-camel-got-its-penis.html?full=true

Symmetry is usually prized as a sign of health and good genes, so why do so many organisms have lopsided genitalia?

BERNHARD HUBER's bespectacled face is just visible behind the piles of vials and bottles that form a skyline on his desk at Museum Koenig in Bonn, Germany. In them float the pickled remains of thousands of daddy-long-legs spiders waiting to be returned to natural history museums around the world. And somewhere amongst them sit a few specimens of Metagonia mariguitarensis. It was this tiny Venezuelan species that first put Huber, a world expert on daddy-long-legs spiders - not to be confused with crane flies or harvestmen - on the untrodden trail of the evolution of asymmetric genitalia.

Spiders, he explains, are among the most perfectly symmetric animals. As anybody with any experience of disembowelling knows, outwardly symmetric creatures are often much less neatly laid out inside, with internal organs jumbled around. Think, for example, of our own loopy intestines, left-sided heart and right-sided liver. Not so the spider. As a rule, its left half is an exact mirror image of the right. That's why M. mariguitarensis was such a surprise when it was discovered in 1986. All male spiders have a pair of sex organs called pedipalps, held like two boxing gloves in front of their face, but in this particular daddy-long-legs spider the right pedipalp was twice as large as the left. For many years, it was thought to be one-of-a-kind.

Strange asymmetry

Although genital asymmetry is extraordinarily rare among spiders, when Huber started looking into the matter it soon became clear that the rest of the natural world is awash with lopsided penises and crooked vulvas. He also realised that from an evolutionary point of view, all this blatant asymmetry is very strange.

The significance of symmetry was only made clear with the discovery that stress and disease make it harder for an individual to develop a perfectly symmetric body. Small differences on either side of an imaginary mid-plane therefore betray genetic quality, and potential mates use this to gauge each other's desirability. Put simply, symmetry is sexy. So why have so many organisms evolved to be asymmetric at the business end of things? That is the question Huber set out to answer.

Insect genitalia are renowned for their complexity. These structures are wonders of biological engineering - sexual Swiss army knives with intricate assemblies of springs, plates and levers. And, as Huber discovered when he started trawling the entomological literature, the bewildering variety of forms includes many asymmetric ones. Entire orders of insects have succumbed to wholesale one-sidedness - male stick insects, praying mantises and cockroaches, for example, always carry skewed genitals. Asymmetric male and/or female genitals also pop up here and there throughout the evolutionary trees of beetles, butterflies and earwigs (Biological Reviews, vol 82, p 647).

Such lopsidedness also exists closer to home. Among vertebrates, we find asymmetric genitals in four families of fish, and also in ducks - where the males often have a helical penis and the female a helical vagina coiled in the opposite direction, possibly to make it harder for unwanted males to penetrate them. Meanwhile, in snakes, the males' two penises are always of unequal size.

Genital asymmetry seems to be particularly common among our closest relatives: in 1974, M. R. N. Prasad of the University of Delhi, India, exposed the wide variety of asymmetries in mammalian penises. The Indian giant flying squirrel, for example, has a helical penis-bone and glans. Male camels and llamas possess two-pronged penises - with a large hook-like finger on the right and a small pointed branch on the left. And the ruminant penis often has a ridge on the right-hand side or is coiled like a corkscrew (Handbuchder Zoologie, vol 9, p 1). Even human genitals display subtle but intriguing asymmetries (see "Classical good looks").

Then there are flowers, which are, of course, the genitals of plants. Back in 1882, American botanist James Edward Todd published a paper in The American Naturalist (vol 16, p 281) in which he reported the curious fact that the Texas tumbleweed Solanum rostratum has flowers with the style - a part of the female sex organ - bent to the left and the male anther to the right, or vice versa. In fact, Charles Darwin's last letter, sent nine days before his death, was to Todd asking for some seeds of this plant so that he might have "the pleasure of experimenting with them". Since then, similar skews have been found in flowers from at least 12 different plant families, says evolutionary botanist Spencer Barrett at the University of Toronto in Canada.

This extravaganza of asymmetry can only mean one thing: in evolutionary terms it often pays to be a bit lopsided in the nether regions. This is puzzling, given all the evidence indicating that the most symmetrical individuals tend to be the most successful at passing on their genes. In recent years, for example, there have been studies showing that humans prefer partners with symmetric faces, barn swallow females preferentially pair with males that have super-symmetric tail streamers, and female zebra finches favour males that have plumage spotted in the most balanced way.

There is even evidence that genitalia are prone to the same scrutiny. When Chiharu Koshio at Naruto University of Education in Tokushima, Japan, kept track of almost 200 female white-tailed zygaenid moths, measuring the genitalia of the males that successfully mated with them and those that were rejected, he found that the chosen ones had more symmetric genitals (Behavioural Ecology, vol 18, p 571).

If symmetrical individuals are preferred as mates then it is difficult to see how asymmetry could begin to evolve. But biostatistician Stefan Van Dongen of the University of Antwerp in Belgium has a solution. He makes a distinction between minor genital asymmetries that are a sexual turn-off, such as in Koshio's moths, and conspicuous ones. The former are the result of "minute errors in following a predisposed growth plan", he says. In other words, they do signal a lack of biological quality. The latter, by contrast, result from drastic alterations of the growth plan caused by genetic mutations that have been selected by evolution. "There are several reasons why genitals would or should evolve to be asymmetric," says Van Dongen.

So what might these reasons be? One turns out to be as mundane as efficient packing. Take the asymmetric daddy-long-legs spiders. Huber's painstaking dissections have revealed that it belongs to a genus in which females have very little space between their uterus and the body wall, so that their reproductive plumbing is always folded and asymmetric. Usually, females exhibit "antisymmetry", which means individuals representing both mirror images are equally common in the population. As a result, there is no benefit for the males to specialise in targeting them from either the left or the right. There is only one exception, M. mariguitarensis, in which all females have their reproductive tract folded to the right. This, says Huber, has led to the evolution of males with a larger pedipalp on the right, allowing them to deliver more sperm on the side where it has a better chance of fertilising an egg.

This "packaging hypothesis" has also been invoked in birds. During the breeding season, males often have extremely large testes, with one bigger than the other. However, when evolutionary ecologist Sarah Calhim of Queen's University in Kingston, Ontario, Canada, and Tim Birkhead at the University of Sheffield, UK, tested the idea, they found something else was going on.

Dissecting 232 male red-billed quelea (a kind of weaver bird that raids wheat fields) that had been killed as part of a pest-control programme, Calhim and Birkhead found that, contrary to expectation, most males had approximately equal-sized testes. However, whenever one was conspicuously larger, the other was correspondingly smaller. Finding the same pattern in zebra finches, they concluded that testis asymmetry, in these birds at least, does not result from optimal packaging, but from compensation: if one testis is damaged or diseased, the other grows to boost its sperm output (Proceedings of the Royal Society B, vol 276, p 2279).

Genitals being what they are, it is not surprising that more titillating explanations for asymmetry have also been proffered. One is based on the discovery that in many species a female can choose whether to store or discard sperm at will, based on her liking of the signals a male gives her during mating.

The idea here is that some penises may have evolved to be asymmetric to stimulate females into extending copulation and using more sperm. This seems to hold true in pigs, where farmers have found that sows artificially inseminated using a catheter resembling a boar's corkscrew-like penis eject less of the costly semen than those inseminated with a non-lifelike catheter. Similarly, in the fly Dryomyza anilis, the more asymmetric the phallic "drumsticks" with which the male taps the genital region of its mate, the likelier she is to use his sperm (Behavioural Ecology and Sociobiology, vol 42, p 185).

Another idea is that genital asymmetry evolved as the result of sexual conflict. Huber thinks that this could explain why it is so common among insects. It's all to do with the position of coitus, he says. The original position - still seen in primitive insects such as mayflies - had the female on top of the male. Later, mating modes evolved that gave the male more control over the female and more possibilities to subdue any attempts by her to escape. In stick insects, for example, the male sits on top of the female, twisting and bending his abdomen to connect with the female from below - something that is aided considerably by his asymmetric penis. More recently evolved insect groups, such as flies and beetles, adopt a similar mating position, but instead of bending their abdomen they have evolved even more drastically twisted genitals to reach inside the female.

Even flowers do it

Many of the explanations of asymmetry invoked for animals cannot apply in plants that fertilise one another using insects as proxies. But even those asymmetric plant-genitals that intrigued Darwin have given up their secret. When Barrett and his student Linley Jesson manipulated Texas tumbleweed flowers by pruning and tying their styles and anthers with nylon thread to make them more symmetrical, they became more likely to self-pollinate (Nature, vol 417, p 707). They conclude that asymmetry in plants helps prevent inbreeding. Bumblebees visiting a left-styled, right-anthered flower will pick up pollen on the right side of their body, with which they are then more likely to pollinate a right-styled, left-anthered flower.

Given the disadvantages of inbreeding, it is surprising that so few plants do this. Other mysteries remain, too. Richard Palmer at the University of Alberta in Edmonton, Canada, seen by many as biology's foremost asymmetry guru, describes Huber's mating-position explanation as "quite plausible" for insects but thinks we still haven't got to the bottom of genital asymmetry in other animals.

Palmer also points out that we know little of what is happening at the genetic level. With any asymmetry two mirror-image forms are possible, but in most species only one of these exists - the camel's two-pronged penis is invariably larger on the right, for example. This suggests that genes force the developing genitalia in a particular direction.

But what about the rare cases where both mirror images exist in the same species? This is the case in the praying mantis Ciulfina baldersoni and the moth Scythris antisymmetrica. Have they done away with those direction-determining genes? Or have they evolved separate gene versions for each mirror image, and if so, why? It cannot be for preventing self-fertilisation, as in the Texas tumbleweed. "That is one of the really big questions," says Palmer.

Once, such questions would have been a minority interest, but increasingly biologists are starting to tackle them. Huber's review has certainly been a spur. And this year's congress of the European Society of Evolutionary Biology in Tübingen, Germany, in August will have a symposium almost entirely devoted to genital asymmetry. Clearly, this is no longer the backwater it was when Huber set out on his voyage of discovery.

Menno Schilthuizen is an evolutionary biologist and science writer based in Leiden, the Netherlands