ONCE upon a time, sex in the animal kingdom seemed pretty simple. Flamboyant male met coy female, male courted female, male deposited spermatozoa in the vicinity of an ovary, then headed out to do it all again elsewhere.
Then biologists began to look more closely, at what really happens. They found that being the biggest and brashest male doesn't always win you mating rights. Among weaver fish, for example, it is good fathers, the ones who will take care of the fry, who get the girl. Females don't always conform to type either. The female bean weevil, for instance, would rather drink her mate's ejaculate than use it to fertilise her eggs. Reproduction, it turns out, is a complex affair.
Just how complex has been emphasised anew with a slew of studies that highlight the staggering diversity of sexual practice in the animal kingdom. Intercourse is a bizarre and often dangerous pursuit, where sexually transmitted infections can be desirable, living in a male harem inside your mate can make sense, and headless lovers give you extra. Relations between the sexes are also surprisingly convoluted. Biologists have charted virgin births, spontaneous sex changes and, perhaps weirdest of all, males who father their brother's offspring. Human sexual exuberance is tame compared with some of the things that animals get up to in the name of reproduction.
Take the male preying mantis, the poster boy of risky sex. In an ideal world, he will jump onto a female's back, establish a rigid grip, copulate and jump away again, safe to repeat the process with some other female. Much of the time, however, that grip will slip. If it does, the male slides within reach of the female's mandibles and he stands a very good chance of having his head bitten off.
Being eaten by your partner during copulation is clearly not desirable. William Brown at the State University of New York at Fredonia thinks the males tread a delicate line. His research reveals that they approach females with trepidation: the drive to reproduce and the drive to survive are at loggerheads (The American Naturalist, vol 167, p 263). "Our work suggests that males actively assess the level of risk posed by an individual female and alter their behaviour to reduce the risk of sexual cannibalism," Brown says. "We expect that the level of acceptable risk to the male will depend upon features such as the availability of safer mating opportunities, the age of the male - and thus his expectation of future reproduction - and perhaps even the quality of the female."
From the female's point of view, cannibalistic sex looks like a winner on several fronts. Clearly, it provides a nutritious meal, making it particularly popular among females who have not eaten for a while. But there may also be another benefit. In some mantid species, losing your head means that you have also lost the system of nerves that tells you to stop copulating. Meanwhile, the nerves that keep copulation going, which are in your abdomen, remain intact. So following decapitation, the female gets everything the male has to offer, as it were. There's just one downside. "Hungrier, more cannibalistic females attract fewer males," Brown says.
Another species in which females keep males firmly in their place is the green spoonworm, Bonellia viridis. Found in the warm waters of the Mediterranean Sea, B. viridis begins life as free-floating flake-like larvae. When they settle on the sea floor, they mature over a period of years into 10-centimetre-long females. Many, however, do not make it this far. If a larva should settle on top of a female instead, she produces a chemical called bonellin that turns the larva into a tiny male. This male then creeps up her body and into her mouth, from where it migrates down to her uterus. "Once inside the female, males assume a parasitic existence: they depend on the female for their nourishment," says Patrick Schembri of the University of Malta. But there is mutual benefit. With up to 20 males safely holed up inside her genital sac, the female can get her eggs fertilised without expending any effort on finding a mate.
With 20 males inside her genital sac, the female green spoonworm can get her eggs fertilised without any effort
While B. viridis females keep their males captive, aphids prefer a more detached relationship. In fact, many species only copulate once a year and it's not even sperm the females are after.
The female green spoonworm keeps the male in its place
(Image: Biosphoto/Dino Simeonidis/Still Pictures)
A female aphid can reproduce without sex. In terms of her genetic legacy, it makes perfect sense to do this because she can produce many clones that carry all her genes down through the generations. So why do aphids make time for an annual bout of sex? This question puzzled Nancy Moran and Helen Dunbar at the University of Tucson in Arizona. Their surprising discovery is that aphids have sex to acquire sexually transmitted infections (
Proceedings of the National Academy of Sciences, vol 103, p 12803).
Infectious sex
Like you and me, aphids carry bacteria on and in their bodies, many of which are useful. Some break down plants the insect would not be able to digest unaided. Others confer resistance to extremes of temperature. One particularly valuable bacterium,
Hamiltonella defensa, kills the grubs of parasitic wasps before they start growing within the aphid's body cavity and consume it from the inside. A female aphid can acquire such useful bacteria by having sex with an infected male, and she can also pass them to her future clones. "Once they are established in the clonal descendants of the sexual female, they can be quite stable and confer longer term resistance," Moran says. So her female offspring will continue favouring asexual reproduction while the males wait on the sidelines for a chance to exchange bacteria for sex.
Aphids
Aphids not withstanding, sex is an extremely popular means of procreation in the animal kingdom. Its ubiquity is still something of a mystery but it must offer benefits that outweigh the advantage of being able to produce numerous exact copies of oneself by cloning. One possibility is that by shuffling your genes and throwing your lot in with another individual, you can produce healthier offspring that do not inherit the damaging mutations that inevitably build up in an isolated genome. Another is that sexual reproduction gives rise to offspring with novel genetic combinations that increase the chances that some will survive when faced with environmental change or disease. But wouldn't it be more useful if, like the aphids, an individual could hedge its bets, switching between sexual and asexual reproduction and getting the benefit of both?
Alas, for most higher animals that is not possible. However, there are some exceptions where cloning occurs via a process called parthenogenesis, where the egg fuses with a by-product of egg production - known as a sister polar body - rather than a sperm cell. This rare form of asexual reproduction has occasionally been observed in lizards and birds: female turkeys isolated from males for a very long time, for instance, sometimes produce young by parthenogenesis. But it seems to come at a price. Mortality rates are high and developmental problems abound.
Which makes a recent report from researchers at the Field Museum in Chicago all the more intriguing. Earlier this year, Kevin Feldheim and colleagues published the results of a genetic analysis of two white-spotted bamboo sharks born in captivity to a mother who had never shared her tank with a male (
Journal of Heredity, vol 101, p 374). The test confirmed that they are clones and that their mother had not experienced a close encounter of the sperm kind. There have been a few reports of virgin births in sharks before now, but none has been known to produce offspring that survived long term. The bamboo sharks are now five years old and healthy, suggesting that parthenogenesis is not an evolutionary dead end after all.
Mushroom coral
Animals that can adapt their sexual strategy to suit their situation are clearly at an advantage. The ability to occasionally do without sperm if there are no males available may be what has allowed sharks to stick around for hundreds of millions of years, making them one of the most ancient animal lineages on Earth. Some creatures have an even more impressive trick, though - when the going gets tough they have a sex change.
Bees do it, some fish do too, but the latest creature to join the list of transsexuals is the mushroom coral. By switching from female to male, it can survive environmental stresses such as temperature rises that cause other species of coral to become bleached and die. "The whole idea is to save energy," says Yossi Loya of Tel Aviv University in Israel, who first spotted this behaviour in 2008 (
Proceedings of the Royal Society B, vol 275, p 2335). The reason is simple - producing eggs costs more energy than producing sperm. So a male-dominated colony is more energetically frugal, increasing its chances of toughing out the hard times. Then, when conditions improve, Loya has shown, some individuals flip between sexes, choosing the one that will give them the best chance of reproducing, depending on what their nearest neighbours are doing.
Ultimate male shirker
The mushroom coral's pragmatic attitude to gender highlights the point that being male is often an easier option than being female. The ultimate male shirker, however, has to be the fire ant - but it pays a price. While the queen and her daughters work tirelessly to keep the colony going, "males are only spermatozoid with wings: they do nothing", says Denis Fournier of the Free University of Brussels (ULB) in Belgium. Even their occasional contributions of sperm ultimately come to naught, since the eggs they fertilise all develop into the sterile female workers. Meanwhile, the queen produces new queens by cloning. In this way, males are cut out of the evolutionary line.
In fact, additional males are only produced when the queen lays eggs that do not contain any of her genetic material and a male fertilises them. This odd situation has led David Queller of Rice University in Houston, Texas, to suggest that the males can be considered a separate species to the females (
Nature, vol 435, p 1167).
If your sole contribution to reproduction is a single, tiny sperm, you are always in danger of becoming expendable, so it makes sense for males to add value. A good ploy is to help raise the kids, but if males are not to waste time and energy caring for someone else's offspring they need to be able to recognise their own. That can be far from simple, as the very strange tale of the marmoset illustrates.
Marmosets
These small South American monkeys are among the most attentive of fathers. Marmosets are born as fraternal twins, developing from two distinct eggs, but they have more in common than your average siblings. From early in gestation they share a placenta, causing their blood to intermingle. As a result, most are born containing cells from their twin, making them chimeras. This has been known for half a century, but it has now become apparent that there is a link between marmoset chimerism and doting dadhood.
In 2007, Jeffrey French and colleagues from the University of Nebraska in Omaha reported that over half of all male marmosets have chimeric sperm, meaning that they are in the bizarre position of being able to father their brother's or sister's offspring. Some females also have chimeric eggs, meaning they may effectively be surrogate mothers for their twin. In addition, many marmosets also have chimeric skin and so produce odours characteristic of both their own genetic make-up and that of their twin. Marmosets recognise each other by these smells, and the researchers found that fathers and uncles are more than twice as likely to look after young with chimeric skin. Mothers and aunts, in contrast, pay less attention to offspring with chimeric skin than to those without.
Over half of all male marmosets have chimeric sperm, meaning that they are able to father their twin's offspring
The implications are mind-boggling. Clearly the marmosets' genes are all mixed up - to such an extent that even the researchers are left scratching their heads over whether these little monkeys should even be considered as separate individuals. Still, in a world where a chimeric male can father chimeric twins with his brother's sperm, surely human relationships will never look quite so complicated again.
How to survive celibacy
Animals have some very strange sexual habits, but perhaps nothing is quite as puzzling as the bdelloid rotifer, which has survived for 80 million years with no sex at all. This ancient line of cloners was seen by the late John Maynard Smith as an "evolutionary scandal". According to standard evolutionary theory they should have become extinct long ago. Without the gene shuffling and novel genetic combinations that sex brings, parasites or changing environments ought to have done them in by now. However, it is now becoming clear how bdelloid rotifers have kept their virginity for so long.
Rotifers
In 2008, researchers from Harvard University and Woods Hole Marine Biological Laboratory, both in Massachusetts, found one trick the rotifers use when they discovered that the creature's genome is chock-full of genes from bacteria, fungi and plants. While bdelloid rotifers may not be swapping genes among themselves, over the millennia they have clearly had a healthy trade via
horizontal gene transfer with other organisms. This, the team suggests, could be a satisfactory alternative to sex, giving a limited means of shuffling genes (
Science, vol 320, p 1210).
Then, earlier this year, a team led by Chris Wilson of Cornell University in Ithaca, New York, found that the canny rotifers have another strategy that might make sex redundant. Rather than fighting their parasites by evolving, they evade them by allowing themselves to desiccate and be blown away on the wind. When they reach another location, they rehydrate and get back on with the business of not having sex (
Science, vol 327, p 574).
"If parasites are indeed the problem that sex evolved to address, then bdelloids may have a unique alternative way of solving it," says Wilson.
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