Return to Genesis of Eden?
Sex and Evolution Mar99
Aggressive female starlings may guarantee higher incidence of mongamy
Your Cheating Heart 21 Nov 98 29
Monogamy and infidelity are not as incompatible as they might seem. Robin Dunbarexplains why it pays to cheat on your partner
UNTIL DEATH us do part. With these words Christianity enshrines the idea that humans are a monogamous species. So why do more than a third of all marriages in Britain and half of those in the US end in divorce? And how come as many as 15 per cent of children are fathered by a male who is not their registered father? Some people see this as a sign of the times: a breakdown in family values, the disintegration of society, or a modern disease that requires everything, including relationships, to be "new and improved". Recently, however, biologists have come up with another explanation. We are finding that monogamy is not a fixed and immutable instinct, hard-wired into some animals'brains, as we previously thought. Even creatures once considered as paragons of fidelity will indulge in a fling if the situation is right. Take the South American marmoset and tamarin monkeys. Both are usually monogamous in the wild, with males largely responsible for bringing up the young. But in some cases, males engage in roving polygamy, hitching up with a succession of females. "Divorce" rates can be as high as a third of all pairs in the population during any one year. This radical change in behaviour is often prompted by an excess of males, usually because of high female mortality. With females in short supply, males who cannot get a mate become "helpers-at-the-nest", willing to assist with the rearing of offspring that are not their own. The presence of a helper increases the chances that a breeding male will desert his partner and go searching for another female because he will be able to breed again sooner than if he waited for his current mate to come back into breeding condition. The helper gets his payoff next time the female comes into oestrus, when he mates with her. And the females seem indifferent to their mate's behaviour: so long as they have a male to help with rearing the offspring, they don't seem to mind too much who he is. The key to understanding what is going on is to look at the benefits of the altered mating strategy. My mathematical models of this behaviour show that, under the right environmental conditions breeding males who are powerful enough to pursue this kind of roving strategy can gain up to twice as many offspring as they would by remaining in a normal monogamous relationship. Females fare no better or worse since either way they reach their optimum reproductive potential, and the helpers make the best of a bad situation. In this case, the new behaviour is a response to a change in circumstances and benefits some of the males. But even without external changes, it may be in the interests of monogamists-both male and female-to adopt a more flexible approach. Indeed, human behaviour is by no means unique. The animal world, it turns out, is full of examples of cuckoldry, cheating and even divorce, by supposedly lifelong mates as they try to overcome what I call the monogamist's dilemma.
Breaking the rules
Monogamy is relatively rare in nature. Only about 5 per cent of mammals are monogamous, with primates and dogs favouring the practice more than most. But there is one group of animals for which monogamy is the rule. Around 90 per cent of bird species pair, at least for a given breeding season. On the surface it looks like the wedded bliss conjured up by the ubiquitous photos of bride and groom. But a decade or so ago, that illusion was blown away when the new technology of DNA fingerprinting revealed that as many as a fifth of the eggs produced by monogamous female birds had not been sired by their regular partners. Many male birds were busily feeding offspring that were not their own. What was going on? Behavioural ecologists who had previously focused on cooperation as the driving force behind monogamy (see "Only you") had to revise their views about mating strategies. They began to see the flip side of the coin: that alongside cooperation comes the inevitable risk of exploitation. A monogamous male can never be sure that he is the father of his partner's young. In cooperative systems, it always pays some individuals to opt for the free-ride strategy by leaving their allies (in this case, literally) holding the baby. That way, they gain all the benefits without having to pay the costs. The monogamist's dilemma is whether to stay with his mate and risk being cuckolded, or to abandon family life and risk losing his own offspring because their mother cannot feed them by herself. He would like to have it all. And in evolutionary terms that means developing sneaky strategies to mate with new females, while finding ways to avoid wasting energy bringing up the offspring of other males. Once the DNA analysis had revealed the extent of extra-pair mating, researchers began to see the mating game for what it was and anti-cuckoldry strategies also started to be noticed. Perhaps the best known example is provided by the humble dunnock, a small and undistinguished looking British sparrow. Nick Davies and his colleagues at Cambridge University have used DNA fingerprinting to show that male dunnocks weigh up very accurately the effort they put into bringing food back to the nest against the number of nestlings they have sired. And how do they achieve this remarkable feat? By the very simple trick of estimating how much time the female was out of their sight during the egg-laying period. That, it turns out, is a very good estimate of the likelihood that she was engaging in a little fling in the bushes with the male next door. Humans are also highly suspicious of extramarital relationships, a fact attested to by the frequency with which separated husbands are now resorting to DNA fingerprinting to avoid paying former wives for the upkeep of their children. And it seems they may be justified. A few years ago, Robin Baker and Mark Bellis, then both at the University of Manchester, calculated that between 10 and 13 per cent of all conceptions in Britain arise from matings with non-pair males. They based their estimate on self-reports of the frequency of double matings-matings with both the normal partner and another male within five days of each other-around the time of ovulation. Both men and women seem, at a subconscious level at least, to realise that paternity may be in doubt. We see this in the comments that people make about newborn babies. Martin Daly and Sandra Wilson at McMaster University, found that mothers and their relatives are disproportionately more likely to refer to similarities between the baby's features and the man's than to the mother's despite the fact that one newborn baby looks pretty much like any other. Humans are caught in the same bind as any other monogamous species. The male wants to monopolise his mate's future reproductive output, but he has to tread a careful line. Mating is ultimately a game of cooperation rather than coercion: too aggressive a policing strategy may well drive the female away. In Californian chuckwalla lizards, for example, very aggressive territorial males achieve fewer matings because they scare females away. Barbara Smuts, of the University of Michigan, Ann Arbor, has shown that overly aggressive male baboons suffer the same fate: females spurn their attentions in favour of socially more skilful males. By the same token, the male's response to suspicions of cuckoldry should not necessarily be outrage. Although a male risks rearing children unrelated to him, he should continue to treat all his partner's children as his own so long as doing so allows him to maintain a satisfactory relationship with her and thereby gain access to most of her future reproduction. Being too inquisitive may backfire by raising doubts in his own mind or by causing his partner to desert him in favour of a kinder rival. Rearing a few offspring sired by another male may simply be the cost some males must pay to reproduce at all. It is easy to see what a male gets from playing away from home, but what does the female gain from acquiescing in an extra-pair relationship? Current thinking makes two possibilities the frontrunners. The first can be described as hedging bets. Ideally, the female would like a male who will invest in her offspring: a man with a bulging wallet, perhaps, or a robin with a large breeding territory She also wants a mate with good genes, a quality which she might assess by looking at his tail if she is a peahen, or by the symmetry of his features if she is a woman. But females usually have to trade one component off against another because the world is imperfect and few males come with high ratings on all dimensions-those that do are usually swamped by suitors. She may try to get the best of both worlds by teaming up with a good provider and allowing him most, but not all, of her conceptions, while allocating the rest to better quality mates as and when she finds them. An alternative explanation for a female's interest in extra-pair males is that it is a way of forcing their pair-male to be more attentive. Magnus Enquist and his colleagues at Stockholm University have used mathematical modelling to show that females can play one male off against another in this way to prevent their pairmale straying in search of other females with whom to mate. But, once again, there is a fine line to tread. Analysis of international data by Daly and Wilson shows that the vast majority of spousal murders in humans are triggered by actual or suspected infidelity. Both men and women often use aggression to try to prevent a mate abandoning them, but sometimes males play their hand too heavily. Even so, intrasexual jealousy seems to be the first line of defence in maintaining the pair bond in many species. In titis, one of the many small monogamous South American monkeys, females are very intolerant of the approach of strange females and will drive them away. And I have observed similar behaviour in a small monogamous African antelope known as the klipspringer.
Maria Sandell of Lund University, studied this experimentally in European starlings. During the egg-laying period, strange females were placed in small cages near to the nest box used by an established wild pair. Males offered the opportunity of a second female showed considerable interest, but their females were rather more aggressive towards the rival. More importantly, Sandell was able to show that females who were more aggressive towards their rivals were more likely to retain a monogamous relationship with their male throughout the breeding season than less aggressive females. Any monogamous partnership is built on tension. Flexible behaviour allows individuals to exploit every opportunity to pursue their needs. So we should not be surprised to see that nature is full of partnerships being dissolved as new and better opportunities come along. Indeed, researchers are finding that "divorce" is common, even among birds that supposedly pair for life, like swans. Estimates of pair-bond dissolution vary enormously, both across species and, within species, across populations. Over half of all pairs of Belgian great tits, for example, get divorced. Andr6 Dhondt, now at Cornell University, Ithaca, New York state, found that not only do females often instigate divorce, but they usually benefit from doing so by subsequently producing more offspring. The luckless males, however, do not always fare so well. Failure to rear offspring is one common cause of avian divorce. Indeed, failure to have children is also one of the highest risk factors for divorce in humans. However, there are as many other routes to divorce in avian society as there are in the human case. Lewis Oring of the University of Nevada, Reno, studies the killdeer, a North American plover. He has found "home-wreckers"-individuals that muscle in on another pair and drive the samesex member out so that they can bond with its mate. Bob Furness of the University of Glasgow has seen similar behaviour in great skuas, a seabird whose ferocious reputation is attested to by the fact that attempts to oust a member of an established pair may result in its death. If there is a message in all this, it must surely be that there are no simple rules that apply to all of the species all of the time. There are some key general principles that apply universally, but pattems of monogamy, divorce and polygamy vary both between and within species in response to local ecological and demographic conditions. But it is the availability of alternatives that makes shifts of strategy possible. Animals, every bit as much as humans, make choices about whom to pair with and for how long, and those decisions are influenced in large part by whether they will do better by staying with the current partner, by moving from one partner to another or by playing a more subtle kind of game.
Robin Dunbar is professor of evolutionary psychology at the University of Liverpool, and co-director of the ESRC's Research Centre in Economic Learning and Social Evolution
Further Reading.. '-The logic of the menage a trois", by Magnus Eriquist and others, Proceedings of the Royal Society London B, vol 265, p 609 (1998) "When birds divorce: who splits, who benefits and who gets the nest", by Susan Minus, Science, vol 153, p 153-155 (1998) "Extra-pair paternity )n birds 1, by Marion Petrie and Bart Kompenaars, Trends in Ecology and Evolution, vol 13, p 52 (1998) ,,Female aggression and the maintenance of monogamy,,, by Maria Sandell, Proceedings of the Royal Society London B, vol 265, p 1307 (1998)
Female starlings who are aggressive owards rivals are more likely to remain in a monogamous relationship.
Natural Born Fathers New Sci 12 Dec 98 38
IT'S ALMOST that time. The baby that was so much fun to make nine months ago is poised to squeeze its way into the world. It's all very exciting, but if friends, parents, midwives and popular self-help books are to be believed, the birth experience is going to be long, arduous, painful work. Especially for you, the father. Your job these days is to be there-encouraging, coaching, empathising and steadfastly refusing to pass out. Can this be natural, ask squeamish dads-to-be. Does it do any good? Or is it just some punishment thought up by feminists? After afl, the males of many species are allowed to sire their offspring and then disappear, off to spread a little more seed. Isn't it enough that human fathers don't eat their young? Sorry, chaps. It's true that genuinely attentive caring fathers are rare in the animal world. But there is a select group of males that are different. They have always made it their business to be around for the special event. And although human dads have only recently been allowed into maternity wards, they seem to be primed for fatherhood in much the same way as these other doting dads. What's more, the harder scientists look, the more paternal participation they find in nature. If anything, human fathers could pitch in a little more. Richard Brown, an ethologist'at Dalhousie University in Halifax, Nova Scotia, was one of the first to realise that the father's presence at the birth matters. He specialises in California mice, Peromyscus californicus, a monogamous species in which both parents share in raising the young. Everyone knew male California mice were caring fathers. Even so, no one had suspected they had a role in the birth. "No one had ever looked for it," he says.
So last year Brown decided to do just that. Working with graduate student Debora Cantoni, he used the lab's video camera to tape a pair of California mice on the big day-or night, as it usually is. They were not entirely sure what to expect. Female gerbils, for example, have the habit of chasing away even the most attentive fathers at some point during a birth. As it turned out, the recording revealed something extraordinary: the male Califomia mouse was better than a midwife. In the lead-up to the birth, he prepared his mate by grooming her and licking her anogenital region. As each of the two or three pups was bom, he helped by pulling it out, licking it off and nesting with it to keep it warm and cosy. Throughout the birth, he groomed and licked his mate. In the end, he joined his partner in dining on the placenta. Brown and Cantoni were astonished. In all the research into parturition, no one had ever ascribed a role like this to the father. So they decided to investigate further. They wanted to know what effect the male presence had-if it made the birth easier, say, or if the pups were more likely to survive. So they videotaped more births, occasionally removing the male two days before the scheduled due date of 34 days, to see what would happen when the female was left to cope on her own. The researchers found that when the male was removed, the birth took almost twice as long-on average 55 minutes, as opposed to 29 minutes when he was around to help. More surprisingly, the father's absence also delayed the start of the birth. "We took the male away and set up the camera," he says. Two days later, when the mother was scheduled to deliver, nothing happened. The next day she still didn't give birth. When males were taken out on day 32, females didn't give birth until day 36-two days overdue, says Brown.
This was all intriguing stuff. "Maybe the male is the stimulus to the female giving birth," he ventures. But how? He tinkered with his experiment a bit more, sometimes putting the male in a separate cage above or even inside his mate's. If the father was giving her some kind of smell signal, she should be able to detect it if he was nearby, Brown reasoned. But whenever the male was not right there, sharing the cage with her, the onset of birth was delayed. Brown and another of his graduate students, Anna Lee, are now looking into what the mechanism might be. Their working hypothesis is that the male stimulates the birth by licking the mother and releasing oxytocin, a hormone known to trigger uterine contractions. Alternatively, says Brown, the delay may be due not to lack of stimulation, but rather to the fact that the stress of being apart inhibits birth for a few days. Whatever the cause, Brown suspects that this effect is not something unique to California mice. "Maybe it's a general phenomenon and no one has noticed it before," he says. He points out that there is a huge variafion in the timing of human pregnancy, too. "One variable might be the absence or presence of the father." Do sailors' wives have different gestations, he asks. What about single mothers? No one has ever bothered to find out. In animals of either sex, something must switch on their parental inclinations at the appropriate time. For the mother, it has always been assumed that hormonal changes during pregnancy bring on matemal behaviour. Prolactin seems to be key. Evolutionarily speaking, it is an old hormone, found all the way up the evolutionary ladder from fish through birds and rodents to humans. It plays a role in hundreds of bodily functions but is best known for the one it is named in honour of: promoting lactation. Studies show that if you block prolactin, mothers stop nurturing and caring for their young; return the prolactin and maternal behaviour resumes. But males don't get pregnant, so what drives them to care about their young? The traditional view is that fathers become paternal when they have contact with their offspring. Brown's work shows that males may be primed for fatherhood even before the birth. Either way, the question remains: what physiological changes lead to paternal behaviour? For a few years, there has been a suspicion that prolactin might be the key here, too. Now there is some evidence to back up this hunch. Katherine Wynne-Edwards and Catharine Reburn, both biologists at Queen's University in Kingston, Ontario, began looking at hormonal changes in male dwarf hamsters around the time their pups were being born. One species, Phodopus campbelli, is biparental: fathers and mothers both care for the young. But a closely related species, Phodopus sungorus, is known for fatherly neglect.
Wynne-Edwards and Reburn reckoned that if pup-to-father contact stimulates the release of hormones which bring on paternal behaviour, then levels should be starkly different in the two species. So she compared blood samples taken from 22 P. campbelli and 16 P. sungorus males-first before they were paired up, and then five days after the birth of their first litter. As she had expected, in the fatherly P. campbelli prolactin levels increased significantly between the two tests, while levels in P. sungorus stayed much the same. Wynne-Edwards and another colleague, Anne Storey of Memorial University of Newfoundland in St John's, speculate that hormones may be at least partly behind paternal behaviour in human males as well. Men's hormones surge and plunge around the time their babies are bom, the researchers have found in a study that is yet to be published. "It's terribly exciting, terribly important. It changes how we view the role of the father," says Sue Carter, a biologist at the University of Maryland in College Park. "These findings suggest there may be a whole shift in the male physiology that allows him to be more reactive, less overreactive." Many textbooks still take the line that hormones don't turn males into caring parents. It's a view that is backed up by some landmark work on rats-but Wynne-Edwards thinks they used the wrong rodent. "The work is beautiful in the rat," she says. "It's just the wrong model." Male rats are not paternal by nature, she says. If you give them enough exposure to pups, or "babysitting experience", as Brown puts it, they can be made to develop parental behaviour. But it does not happen all on its own.
Species that are naturally biparental are different, agrees Toni Ziegler, from the Wisconsin Regional Primate Center in Madison. In every one that has been studied to date, hormones have been linked to parenting behaviour of males as well as females. Ziegler's own work even helps explain Brown's finding, that males may become primed for parenthood before their offspring arrive. She has been studying cotton-top tamarins-the "dads of all dads". Among these monkeys, Saguinus oedipus, fathers are the main caregivers, doing up to 80 per cent of the rearing of the infants. Males take on almost all the tasks that don't involve nursing, says Zieglerwhich is a lot of work, considering cottontops tend to be born in twos and threes. "Almost from the moment of birth," she says, "the mother will allow the father to take the twins." Mum, on the other hand, spends most of her time eating and promenading. Since she will typically ovulate within two weeks of giving birth and probably conceive again then, she needs to preserve her strength for reproduction. The older offspring usually hang around and help out for a few years before striking out to start families of their own-and it's mainly the young males that are keenest to lend a hand. Ziegler measured levels of prolactin in tamarin fathers both during gestation and after the birth of their young. In keeping with findings in other biparental species, she found that following the birth, fathers had elevated prolactin levels-just as high, in fact, as their nursing mates. interestingly, eldest sons also had higher prolactin levels than other single males, perhaps due to their babysitting activities. Among males, the most experienced 8 fathers had the highest levels of the hor-6 mone. In fact, the mean level of prolactin for each male is highly correlated with the number of previous births he has experienced as a father. The paternal highs tended to stay elevated for six weeks after the birth, and never quite dropped back to the levels of non-fathers.
But what Ziegler found in cotton-top tamarins before the birth was even more
surprising. Two weeks before parturition, she detected a prolactin surge in the
fathers that was nearly as high as the one after the birth. It's well known that
females experience hormonal changes around birth. High levels of oestrogen and
progesterone during pregnancy unleash prolactin. But what could trigger such
changes in males? "It's not just the infant that is promoting the prolactin,"
says Ziegler. She suggests that there might also be some kind of interaction
between mothers and fathers in the lead-up to the birth. Could it be pheromones,
or even behaviour? Indeed, her latest work suggests that whatever it is that is
telling males to expect the pitter-patter of tiny feet, experienced fathers seem
to respond more quickly than inexperienced ones. Ziegler is looking at prolactin
levels in male cotton-top tamarins throughout their mates' six-month gestation
period. Her preliminary findings are intriguing. In fathers who'd already had a
few batches of twins, prolactin peaked early, at around month two or three,
whereas first-time fathers were slower to catch on; their levels did not peak
until well into the fifth or sixth month. This suggests that the response is not
simply instinctive. "We're wondering if experienced fathers are just
perceiving better," she says. Wynne-Edwards is also keen to find out how
mothers and fathers communicate in the lead-up to birth. She points out that
some birds send signals back and forth during gestation. "I think we'll
find in mammals that prolonged contact and cohabitation is really
important," she says. "The male goes through changes in pregnancy
alongside his mate," says Wynne-Edwards. So maybe those annoying men who
chirp "We're pregnant" aren't so far off the mark after all.
Like a Virgin New Sci Xmax 98 36
WELCOME to the farm where the mating season never comes. Here the ewes, cows and sows form a celibate sisterhood, yet somehow they manage to carry on the business of procreation anyway. Without testosterone-pumped suitors. And sans sperm. Each year, they spawn another generation, all female, all with impeccable genetic credentials, because long ago scientists helped to purge their lineage of destructive mutations. This farm is the futuristic vision that virgin births were supposed to build. That was the view from 1957, when geneticist Richard Beatty of the University of Edinburgh published a book on the scientific study of parthenogenesis-the development of an embryo without the help of sperm. He argued that creating generation after generation of virgin-born mammals would not only help to improve and accelerate the breeding of livestock (producing big males for the sake of a little sperm slows down breeding), but would yield new insights into disease, genetics and the function of sex itself. Today, the pursuit of fatherless propagation by farm animals seems bizarre. But before words like "genome project" and "DNA diagnostics" were ever uttered, biologists were betting that parthenogenesis would help them to change the world.
The search for a mammalian virgin mother has gone through many incarnations since those days: from a great hope of agriculture to the obsession of top reproductive scientists, from an impossible dream to the reality of sex-free replication with the help of cloning technology. And although the world is unlikely to change as dramatically as Beatty once envisaged, it may soon be possible to genetically engineer mammals that reproduce purely through parthenogenesis. Of course, asexuality was hardly a new idea. The ability of microbes, insects and plants to reproduce without a hint of carnality was well known. But pioneering experiments in the 1920s and 30s had raised a new question: just how far up the evolutionary tree had parthenogenesis managed to climb?
Some evidence suggested it might have reached the very top. Scientists discovered that in the ovaries of vertebrates, even in some mammals, eggs would occasionally begin to develop without a whiff of sperm about. There were even isolated reports that these parthenogenetic embryos could develop into full-blown animals. "This work turned out to be dead wrong," says Christopher Graham of Oxford University, whose own studies of parthenogenesis in mice began in the 1970s. "But they made for very exciting, optimistic times." No episode reflected this optimism better than when geneticist Helen Spurway from University College, London, unintentionally sparked off a serious hunt for a human virgin birth. In 1955, she argued that virgin births might be discovered most easily in humans. She said that women who suspected they had parthenogenetic children might be encouraged to step forward if they knew that their claims could be vindicated beyond a reasonable doubt. She pointed out that science made some clear predictions for a human virgin birth. Biblical precedent apart, the infant bom of mammalian parthenogenesis should be female. Mammalian sex is determined by the X and Y chromosomes. Males are XY, females XX. Since a mother's egg can only contribute X chromosomes, the child must be XX. And this child could only have genes that her mother also possessed. The Sunday Pictorial newspaper repeated Spurway's musing and called for any woman who believed she had given birth to such a child to step forward. Accordingly, 19 women were marched to a bloodtyping specialist, one S. Balfour-Lynn, to substantiate their claim. Most were easily discounted after a few tests showed a blood protein mismatch between mother and daughter. However, an impressed BaffourLynn reported in the medical journal the Lancet that one daughter matched her mother on 14 different genetic criteria. This mother's claim must not only be considered seriously, Balfour-Lynn concluded, "but it must also be admitted that we have been unable to disprove it". if he'd had the knowledge of modern immunologists at his finger tips, BalfourLynn would have been far less impressed. For instance, his potential virgin mother had rejected a skin graft from her daughter after several weeks. This was slow for tissue rejection and an "obscure" finding to the esteemed blood specialist. But it is now clear that rejection, however long it took, showed that the daughter had genes the mother did not, and meant sudden death to a claim for parthenogenesis. Evidence for parthenogenesis in other mammals was also unravelling. For example, many laboratories were unable to reproduce perhaps the most impressive claim of the 1940s, the production of parthenogenetic rabbits.
But there was enough good news to keep some top scientists interested. In the late 1950s, American and Russian researchers tracked down populations of all-female lizards that reproduced exclusively by parthenogenesis. Meanwhile, researchers in the US made a discovery that brought virgin births closer to home, and closer to the dinner table-parthenogenetic turkeys. Beginning in 1952, Marlow W Olsen and his colleagues at the US Department of Agriculture in Beltsville, Maryland hatched 1100 parthenogenetic turkeys. The group found that a talent for fatherless development was strangely common in some breeds of turkey, where up to 40 per cent of eggs developed without sperm. About 1 in 5 of the birds that hatched was fertile. Perpetuating the lineage by parthenogenesis was a little difficult, however, because all the offspring were male. That's because sex in birds is determined by a different set of chromosomes to mammals, called Z and W Males are ZZ and females ZW. Because of the way the eggs develop, parthenogenetic embryos have only one type of sex chromosome, and of the two possibilities only ZZ embryos can survive. The turkey's odd reproductive ability is often dismissed as a quirk of extensive inbreeding during its domestication. But Tom Savage, a turkey researcher at Oregon State University in Corvallis, points out that it might be useful in the ' wild. If female turkeys are inseminated with semen low in sperm, for example, the incidence of parthenogenetic egg production goes up. The incidence also increases if the birds are infected with viruses. This suggests that virgin births are a response to any threat to the she-turkey's chance of successful sexual reproduction. In fact, another instance of parthenogenesis that produces only male offspring was reported just over a year ago by David Chiszar at the University of Colorado, Boulder, and Gordon Schuett of Arizona State University West in Phoenix (This Week, 27 September 1997, p 23)-in a virgin timber rattle snake. Since then, the researchers say they have found evidence that other snakes may occasionally adopt the same type of reproduction, as might the green iguana and-appropriately enough-certain species of the Basilisk lizard, which is sometimes called the "Jesus Christ lizard" for its ability to walk on water. Chiszar and Schuett argue that parthenogenetic reproduction has played an important role in the evolution of these reptiles. "If a female gets isolated and there is little chance of her mating, this is plan B," says Schuett Even with the few examples of vertebrate parthenogenesis available in the 1970s, some researchers were undaunted. If our feathered and scaly friends could pass on their genes without bothering with sex, surely mammals could pull off the same trick. Hopes rose when Graham and others showed that mouse eggs could be stimulated to begin spermless development in test tubes by treating them with chemicals, enzymes, temperature shifts or electric shocks, which meant the process could be studied in the laboratory. "This began a really enormous effort to produce parthenogenetic mice," remembers Davor Solter of the Max-Planck Institute for Immunology in Freiburg, Germany. But progress certainly wasn't easy. "No matter what we did, the embryos stopped developing during gestation," says Azim Surani of the Wellcome and Cancer Research Campaign Institute of Developmental Biology and Cancer Research in Cambridge. "Understanding why became an obsession." One possibility was that most parthenogenetic embryos inherit a deadly combination of genes. This poor genetic legacy would not be surprising because of the effect of lethal recessive genes. These genes are only deadly if the embryo inherits two copies, one from each parent-usually a rare event. But parthenogenesis can be thought of as a highly inbred mating between the egg and itself. So in parthenogenesis, the probability of inheriting any recessive lethal trait is much higher than for the offspring of two parents. This was both good and bad news for parthenogenetic enthusiasts. It meant that if generations of parthenogenetic mice could be produced, their lineage would quickly be cleansed of any deadly traits. But equally, if a strain contained several recessive lethal mutations, a parthenogenetic lineage wouldn't have much chance of succeeding. So the researchers devised a clever new way to "mate" genetic material from different animals, which gave them more genetic freedom than parthenogenesis. A recently fertilised mouse egg contains mum and dad's chromosomes in separate compartments called pronuclei. Both research groups leamt how to remove pronuclei and switch them with pronuclei from other embryos. This meant they coldd "mate" pronuclei from two unrelated female mice, or two unrelated male mice, which should have e@ated any problems with inbreeding.
What they discovered seemed to sound the final death knell for mammalian parthenogenesis. Only when pronuclei from both sexes were present could the embryos complete development. This led to a remarkable idea: that male and female mammalian chromosomes are somehow marked or "imprinted" differently, so that either genome by itself is incomplete ("Hidden inheritance", New Scientist, 28 November, p 27). They reasoned that organisms with a gift for parthenogenesis must lack imprinted genes. Sure enough, among vertebrates, imprinting appears to be exclusive to mammals. Solter also thought imprinting might explain why the cloning of adult mammals hadn't been accomplished. In cloning, a single cell from an animal is persuaded to begin development again to produce the original organism's genetic twin. But Solter reasoned that if essential parental imprints were lost during development, cloning would become "biologically impossible". Now, after the successful cloning of Dolly the sheep in 1997, followed by the cloning of adult cows and several dozen mice reported in the past year, it is clear that Solter was mistaken-but only in part. Researchers now believe that some adult cells probably retain their imprints throughout development. In that sense, Dolly and company didn't overcome the sexual imperatives introduced by imprinting. They simply borrowed imprints from the previous generation. With mammalian parthenogenesis a lost dream, biologists like Surani and Solter began to study its nemesis-imprinting. Beginning in 1991, researchers uncovered the molecular basis of imprinting: certain genes are switched on in sperm, but not in eggs, and vice versa. There are now more than two dozen such sex-biased genes known in manunals. This genetic division of labour thwarts parthenogenesis, but that's probably not why it evolved. Some think that the evolution of the placenta somehow required the activity levels of certain genes to be drastically reduced and that imprinting was a way to achieve this. Because this tissue is a purely mammalian invention, this would explain why other vertebrates didn't evolve imprinting. Another theory, developed by David Haig of Harvard University and his colleagues, is that imprinting is the result of an evolutionary battle between the sexes. When it comes to the growth of a man-woman fetus, each parent has a different agenda. It is in the father's best interest for his offspring to grow large and use up the mother's resources, so they won't be wasted on another male's offspring. Such favouritism doesn't benefit a mammalian mother, however. To her, the unconstrianed growth of the fetus could be deadly. She is better off treating each embryo equally. The result, Haig says, is a genetics arms race, with patemal genes beefing up the offspring and matemal genes attempting to keep growth in check. According to this theory, the development of parthenogenetic embryos fails because they contain a double copy of matemal genes without patemal rivals to act as a counterbalance. "This is a tug of war," says Rudolf jaenisch of the Massachusetts Institute of Technology. "So if one side stops pulling, things are thrown into a sudden crisis." Some genetic evidence bolsters this theory. For example, the gene for insulinlike growth factor 2, Igf2, is expressed in sperm and promotes embryonic growth, while the egg expresses Igf2r, a gene that codes for a protein that inhibits the growth factor. So when researchers genetically engineer mice without lgf2r from their mum, the embryo grows excessively large and dies before birth, while mice lacking the growth factor from their dad are runts. Intriguingly, embryos with neither gene are of normal size and fertility. Jaenisch explains this using the tug-of-war analogy; the battle can end peacefully, so long as both sides drop the rope at the same time. Which leads Jaenisch to a remarkable conclusion. If biologists reverse millions of years of evolution by eliminating imprints from mammalian genes, development should proceed without a hitch.
Brains and brawn
Jaenisch has already tested his theory using mouse embryonic stem (ES) cells, which have the capacity to become any tissue when injected into a normal, developing mouse embryo. The researchers stripped these ES cells of all imprinted markers. With data yet to be published, the researchers show that when these cells are added to a developing embryo they transform into many tissues, including brain (the formation of which requires maternally expressed genes) and muscle (which requires paternal genes). But in that experiment, the ES cells were in the company of normal, imprinted cells in the embryo which may have assisted their development. Jaenisch now wants to go one step further by using the unimprinted ES cell in a cloning experiment like the one that produced Dolly. Because the resulting animal would have come from a single cell, it would have to develop in the complete absence of imprinted genes. If this creature is viable, this would be the strongest proof possible that Haig's theory is correct. And if that experiment works, jaenisch will be only one step away from fulfilling Beatty's vision of producing generation after generation of parthenogenetic mammals. To make the lack of imprinting heritable, the researchers would only have to cripple the as-yet undiscovered proteins that imprint the genes in the developing sperm and egg. "Then you would have animals that could replicate through parthenogenesis forever," says jaenisch. Philip Cohen
Go West, Young Woman New Sci 31 Oct 98 11
Females may have wandered the globe, spreading their genes
FROM Marco Polo to Alexander the Great and Genghis Khan, our image of explorers has traditionally been one of brave men striking out into the wilderness. But a new study of DNA comes to the surprising conclusion that women have historically travelled farther and more frequently than men, and may be more responsible for spreading genes around the globe. Researchers can study the migration of past generations by comparing DNA from people in different countries, taking natural mutation rates into account. To simplify matters, many geneticists have concentrated on mitochondrial DNA (mDNA), which is only passed down from the mother. But over the past few years they have also started to look at the Y chromosome, which only comes from the father ("All About Adam", 11 July, p 34). Mark Seielstad of the Harvard School of Public Health in Boston, along with Eric Minch and Luca Cavalli-Sforza at Stanford University in California, decided to compare the worldwide diversity of the Y chromosome with that of mDNA to see whether different patterns of migration emerged for men and women. They took previously published information on variations in MDNA within populations and between continents, and compared it with Y chromosome data from men in 54 populations from Africa, Oceania, Asia, Europe and the Americas. For MDNA, there was much more similarity between populations than for Y chromosomes, suggesting that women had a much higher migration rate than men. Calculations revealed that the migration rate for women was eight times greater than for men, they say in next month's Nature Genetics (vol 20, p 278). The reason for the large difference is unclear. Seielstad believes that marriage traditions may have played a role-men have often travelled to find wives and returned home with them. "It sounds like a sort of feminist take on things, that women migrate more, but the irony is that it's only because the patriarchal system forced them to move," he says. "It's intriguing that you see this difference on the large scale," comments Mark Stoneking, a molecular anthropologist at Pennsylvania State University in University Park. "It points to a very interesting area for future research." He suggests that computer models might be able to pinpoint the extent to which marriage traditions could explain the global genetic similarity in MDNA. Another possible explanation for the results is polygamy. Polygamous cultures would naturally have less variation in Y chromosomes than other societies. But even in populations where polygamy is considered ideal, few men have the resources to support many wives, so Seielstad doubts whether polygamy could account for the entire eight-fold difference. Steven Strogatz of Cornell University in Ithaca, New York, points out that not many women would need to travel long distances for this effect to occur. He has shown that only a few connections between farflung groups of people can result in apparently unrelated people having friends in common-the so-called "smallworld effect" (This Week, 6 June, p 7). "It probably requires only a tiny minority of women making enormous journeys to globalise their mDNA-that's the essence of the small-world effect," says Strogatz. "But surely a few men have made some long travels too, so we still have to explain why there's such a dramatic gender difference." Nell Boyce, Washington DC
OUT OF AFRICA, INTO ASIA
Controversial DNA studies link Asian hunter-gatherers to African pygmies Sci Am Jan 1999 14
Scientists may have pinpointed direct descendants of the first humans to migrate out of Africa into Asia. They could be the aboriginal inhabitants of the Andaman Islands in the Bay of Bengal, who have long been noted for their resemblance to African pygmies. Some convergence of featuresdark skin and small, gracile form-is to be expected in peoples who have evolved in the tropics. But a recent DNA study of hair from Andamanese individuals, collected in 1907 by British anthropologist Alfred R. Radcliffe-Brown, suggests a closer connection. Carlos Lalueza Fox, a postdoctorat fellow at the genetics laboratory of Erika Hagelberg at the University of Cambridge, had extracted DNA from 42 out of 70 hair samples and amplified a short segment of DNA from the mitochondria. Known as mtDNA, such DNA is less directly related to physical characteristics than chromosomal D and is therefore believed to be less sensitive to the pressures of natural selec tion. Fox and Hagelberg found that th sequences of base pairs in the mtDN fragments clustered closer to Africa populations-especially southern Africa pygmies-than to Asian ones. If substantiated, the findings will len support to the Out of Africa theory o human descent. Proponents hold tha the first humans left Africa som 1 00,000 years ago, reaching Asia aroun 60,000 years ago. According to Pete Bellwood of Australian National Uni versify in Canberra, some of thes hunter-gatherers moved southward t New Guinea and Australia during th ice ages 40,000 years ago. At the time glaciers had sucked water out of th oceans, lowering the sea level and ex panding Asia into a vast region know as Sundaland. As a result, much of the southward migration occurred on foot.
Archaeological evidence of human occupation of the Andamans, excavated most recently by Zarine Cooper of Deccan College in India, dates back at most 2,200 years. But Bellwood guesses that the Andamanese reached their islands during the first wave of human migration at least 35,000 years ago. Eventually the seas rose, cutting them off. The seas were to fall and rise many more times, most recently about 10,000 years ago. kndamanese mythology describes violent storms and deluges that drowned the islands, forcing the survivors to repair to the former hilltops. Almost all the first humans in Asia were wiped out by waves of later migrants; survivors persisted only in isolated, embattled pockets. The Andamanese ensured their own survival-at least unfil modern times-by determined opposition to all seafarers who attempted to land. To this day, one group of Andamanese, inhabiting tiny North Sentinel Island, attacks with arrows any approaching boats. The Out of Africa theory has also received recent support from an extensive survey of Chinese DNA conducted by Li jin of the University of Texas at Houston and his colleagues. The researchers examined DNA markers called microsateflites from 28 ethnic groups across China, including four from Taiwan. They found only minor genetic variations among the population s, suggesting that these groups had had hide time to diverge from one another. Possibly, they all arose from recent African migrants. A rival scenario derives from the Multiregional hypothesis, which holds that humans evolved separately in different parts of the world from populations of Homo erectus that dispersed (also from Africa) one to two million years ago. These groups of humanoids managed to develop into a single species-H. sapiens-by exchanging genes with one another. To some anthropologists, fossils excavated in China suggest a continuum between H. erectus and modern Chinese peoples. Nfilford Wolpoff of the University of Michigan has pointed out that interbreeding could have ensured that the descendants of different humanoids ended up being genetically si-inilar. Wolpoff is likewise skeptical of the Andaman study, which cannot be properly critiqued until it is published. An unfortunate dispute regarding the hair has held up publication. Robert A. Foley, director of the Duckworth Collection at Cambridge, which owns the hair, has complained that permission was never obtained for its use. Hagelberg protests that Foley knew about the study for at least a year before voicing this objection when the results were reported at a conference in August. Matters became so unpleasant that Hagelberg has packed up her lab and moved to the University of Otago in Dunedin, New Zealand. The research will be difficult to rephcate, because fresh materials from the Andamanese are scarce. Access to blood, hair and other human samples is restricted by many countries (in this case, India) for fear that the genetic information they contain will be misused-specifically, put to commercial use. So it will be a while before the intriguing links between Andamanese and Africans strengthen into familial bonds. -Madhusree Mukeijee
The Female Gene New Sci 6 Feb 99 9
THE ASSUMPTION that we'd all be female were it not for genetic switches activated in the womb has been challenged by the discovery of a gene that facilitates female development. It is true the male half of the population would have been female but for a special signal sent out by the Y chromosome in a fetus. But scientists have now found a gene that needs to be switched on for female sexual organs to develop normally. The discovery has prompted one sexual development specialist to rethink the causes of ovarian failure in some of his patients. Mammalian embryos start off sexually neutral. In embryos with an X and a Y chromosome, a gene on the Y that codes for the testis determining factor SRY activates the male developmental pathway. If the SRY gene is defective or if the embryo is female, with two X chromosomes, ovaries and a female reproductive tract form by default. So Andrew McMahon and colleagues at Harvard University in Cambridge, Massachusetts, were surprised to find that female mouse embryos with a particular mutation develop portions of the male reproductive system. "There is no reason to have expected this," says McMahon. Seppo Vatnio, the scientist on the team who made the discovery, bred mice with a defect in the Wnt-4 gene, which codes for a signalling protein. Wnt-4 is normally active in the fetal kidney. Without it, the kidneys do not develop and the mutant mice die soon after birth, because they cannot filter toxins from their blood. But Valnio noticed that the mutant female mice also had differences in their reproductive system, parts of which develop from the same cells as the kidney. As the team reports in this week's Nature (vol 397, p 405), the Mullerian duct, a tube in the fetus which should have grown into the uterus and vagina, lay dormant. The Wolffian duct, a precursor to the sperm-carrying vas deferens had matured instead. Although ovaries in the females lacking Wnt-4 developed in the right place, they had certain testis-like features. Also, cells in the mutant ovaries begun secreting testosterone in the fetus, as testes would. The researchers say the testosterone may account for the development of the Wolffian duct, although not enough was present to affect the external sexual organs, which were female. Eric Vilain, the specialist in abnormal sexual development at the University of California at Los Angeles who discovered that mutafions in SRY gene lead to feminisafion, sees the discovery as part of a trend. "What's interesting is this shift from being obsessed with the testis to becoming more interested in the ovary," he says. "There must be a very complicated pathway leading to the formation of the ovary, and we don't know anything about it. Rather than resulting in a change of sex, damage to genes needed for the female reproductive system rarely causes symptoms until adolescence, when menstruation fails to begin-a condition called ovarian failure. "It's the next hot topic in sex determination," Vilain says. He plans to check the Wnt-4 gene in his patients whose ovaries have failed. Jonathan Knight
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