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Sister are Doing it for Themselves New Scientist 17 Aug 96

THE creatures that inhabit Matthew Meselson's lab at Harvard are every gossip columnists'worst nightmare. It's not just that they're obscure pond-dwelling invertebrates. Or that they have protruding jaws, hairy mouths and scary little eyes. Or even that you need a microscope to see what they're up to. No, it's worse than that. The bdelloid rotifers (to name names) have never been known to have sex.

But then, they never feel the need to. The reproductive systems of these unprepossessitig creatures produce eggs programmed to divide and develop into embryos, unaided by sperm. Each bdelloid birth is a virgin birth. Each new bdelloid is a genetic clone of its mother. And as for the poor old bdelloid males... there aren't any. In human terms, all quite unthinkable (whatever the Vatican might say). Yet in nature as a whole virgin births are not so outlandish. From budding yeast cells to aphids to snails, plenty of species alternate cycles of sexual reproduction with periods when the females give up on the males and simply clone themselves.

Some go the whole hog and reject sex (and males) more permanently. But few organisms have embraced the virgin lifestyle so completely or successfully as the bdelloid rotifers. And therein lies their notoriety, for in evolutionary biology these days it's persistent sexual abstinence, not promiscuity, that's generating all the gossip.

Most multicellular species that quit sex in favour of cloning become extinct within tens of thousands of years, a blink of the eye in evolutionary terms. But the bdelloids seem to have renounced mates tens of millions of years ago. Since then, moreover, they haven't just survived without sex. They have positively thrived, diversifying down the ages into more than 360 species, none with any close sexual relatives. And it's this, the bdelloids' longevity without sex, that has got researchers like Meselson itching to uncover the secret to their evolutionary success. If sex-and the shtiffling of genes that goes with it-is the vital spark of Darwinian adaption, why so many sexless bdelloids? "The arguments for or against the adaptive value of sex are right now in a state of real flux," says Meselson 'You can't dogmatically say you have to have it to maintain biological diversity. 11

Nor, it turns out, are the bdelloid rotifers the only sexless organisms that seem to have dug their evolutionary heels in and survived against the odds. Judging from the fossil record, the Darwinulid ostracods, members of a dynasty of obscure freshwater shellfish species, have had little truck with sex for the past 70 million years or more, preferring to brood their young asexually in a pouch. And evidence from DNA studies points to another member of nature's elite club of "ancient virgins": Artemia parthenogenetica, a shrimp found in salt-rich waters which has survived for at least 30 million years. For biologists, such ingrained disdain for sex is not just an enigma: it's an enigma wrapped in a mystery. And the mystery is the purpose of sex itself. Everyone believes sex must be good for something (why else would it exist?). But what exactly? The key is that on paper at least, populations can grow twice they dispense with males, which slow things down cause they produce no eggs, and embrace cloning instead. in fact, a single cloning female can-again, in theory-produce enough descendants to outcompete a one-million strong population of males and females after just 50 generations. Whatever genetic dividend sex produces, it must kick in fast. otherwise cloning would be the norm. "Sex has nothing to do witli facilitating long-term ev6lution," argues Alexey Kondrashov at Cornell University in Ithaca, New York, a leading thinker in the field. "Its advantages must be short term." But again, what? In the past couple of decades, two ideas have emerged as towering frontrunners, neither of them romantic. Sex may enable species to survive parasites, or perhaps it helps species get rid of harmful mutations in th genes. Then again, perhaps sex does both of these things. SO far, essential data for testing key elements of these thories have been thin on the ground or completely non-existent. The mystery of sex has prevailed. Undaunted, biologists are now making a new assault, this time armed with information about the genetics and biological lifestyles of organisms like the bdelloids. The idea is to use the enigma to solve the mystery: to work out what's special about the DNA and environments of these ancient virgins that lets them survive without sex. For Meselson and his Harvard colleagues, that means figuring out what all those millions of years of sexual abstinence liiive done to the bdelloids' genes. And others are watching their progress like hawks, 'The bdelloids provide a natural testing ground for theories of sex," says Laurence Hurst, a Cambridge geneticist and expert on the evolution of sex. 'Any successful theory must explain not just why most organisms do have sex, but why some don't." ' But sex wouldn't be sex without a scandal, and some people believe the ancient asexuals are not quite what they seem. Delve deeper into the genetics and life cycles of some of these creatures, they say, and you will find they are slyly having sex. Or that their reproductive systems are shuffling genes by unconventional mechanisms. Or that their asexuality is disappointingly short-lived, going back tens of thousands - but not millions-of years.

Secret trysts

In nature, there may be no genuinely ancient virgins, only frauds, warns Paul Hebert, an evolutionary ecologist at the University of Guelph in Ontario. Hebert's own work on fresh water invertebrates like the ostracods has led him to expose a number of fraudulent virgin species over the years. "Many of the ostracods we looked at seemed to be anciently asexual," says Hebert. 'But when we studied them in more detail the Sexual relatives popped up.' Some of the asexuals turned out to be nothing more than short-lived evolutionary 'off-shoots" of these sexual lineages. Other virgins were in fact having sneaky trysts with sexual neighbours. And from aphids to molluscs to salamanders, that same story has been repeated time and again. Indeed, Hurst and his colleagues have even invented a term for it - 'covert sex". Now, covert sex is turning out to be even more common than biologists thought, according to DNA studies that reveal a species' sexual history. The fungus Coccidioides immitis lives in the semi-arid soils of states like California and causes "valley fever' in humans. Symptoms rarely progress beyond a flulike condition but can tum nasty: every year the disease kills 50 to 100 people in the US. Medical mycologists would dearly like to cross different strains of the funjus to identify the genes that influence its virulence. The snag is that the fungus has never been caught producing the sexual spores or fruiting bodies that are the hallmark of sex in fungi. But indulge in sex it does, says molecular geneticist Austin Burt, now working at Imperial College, London. Last year, with mycologist John Taylor and his team at the University of Califomia at Be]Fkele Burt examined DNA samples looking for evidence of DNA exchange between individuals. The researchers found it-in spadefuls. How and where valley fever fungi exchange DNA is still unclear. But Burt suspects the fungus only enters the sexual life cycle underground in the desert habitat far from prying eyes. Since one in five fungi have no visible Sex lives, covert sex could be commonplace. No wonder some fear for the asexual credentials ot organisms like the bdelloids. It takes two to tango, however, and in the 400 years since bdelloids were first described by naturalists nobody has ever reported seeing a male. The only known fossils are a dozen or so bdelloids clinging to the gills of a mushroom entombed in 40-million-year-old amber, and even these look reassuringly like present day females.

Nonetheless, negative evidence seldom wins hearts and minds in scientific debates. And the painful truth is that the discovery of just one male bdelloid, fossilised or alive, would instantly tarnish the bdelloid's reputation and dent biologists' hopes of using these ancient virgins to crack the mystery of sex. Chivalrous help is at hand. Meselson and his team have come up with DNA test to establish that no living species or their evolutionary ancestors have swapped genetic material through sex. It's a test for virginity on an evolutionary timescale, and it works by examining the sentences of closely related genes in individuals. In sexual species, chromosomes and the genes they carry tend to come in two versions, one inherited from each parent. The DNA sequences of the two versions are normally almost identical. And it's sex that keeps them that way. During sexual reproduction genetic material is exchanged between pairs of genes. This means, in effect, that over time both genes end up sharing any random mutations or changes that occur in either one of their DNA sequences: the genes evolve in unison. But asexual reproduction permits no such exchange of genetic material. So when species abandon sex, the sequences of their paired genes may drift apart, each clocking up different random mutations. After millions of years without sex, such species should be rife with these estranged gene pairs. So far for bdelloids these credentials for ancient asexuals have been borne out. The researchers have examined versions of four genes found in a number of rotifer species. In sex-loving Monogont rotifers, each version is virtually identical. But in the apparently sexless bdelloid rotifers, they differ by as much as 10 per cent. Before Meselson and his team crack open the champagne, however, they must resolve a complication arising from the fact that the bdelloids carry genes in sets of three or more, rather than in the more normal pairs. "That's where were stuck right now," laments Meselson. Some researchers, though, are clearly getting impatient. Already, papers seeking to explain how organisms like the bdelloids could survive without sex for so long are surfacing in the journals. Definitive answers are lacking, but valiant theories and inspired speculations abound. What follows is a rough guide to surviving without sex based on some of these.

Dodging parasites

One of the two big evolutionary ideas about sex sees it as the key to breeding resistance to parasites. Without it, the theory goes, we would all be so genetically uniform that diseases would rip through our populations like pests through a crop monoculture (see "is sex good for anything?" New Scientist, 4 December 1993, p 36). So here's the first tip for an aspiring young asexual: beware parasites. And one way to avoid getting wiped out might be simply to keep running. According to computer simulations by Olivia Judson, a theoretician formerly at Oxford, and her colleagues, asexual organisms can beat the odds by dispersing to pastures new whenever the local strains of parasites threaten to wipe them out. It's a hypothesis that seems to chime with certain aspects of the biology of sexless organisms. Evolution has thrown up few doggedly ancient asexuals like the bdelloids but plenty of flyby-night dabblers of more recent origin. And intriguingly, the number of such species increases as you move from the teeming tropics to more sparsely populated temperate latitudes. Tliat could be because it's easier for organisms to evade parasites in less crowded environments. It's clear too that asexuality thrives in the ranks of life's simpler organisms, unicellular protozoa, algae and the like. Because they split in half to reproduce, such organisms have the chance to dump all their parasites onto one cell when they divide, points out Hurst. Other tactics for dodging parasites seem to include living at high altitudes or in water. Asexual plants are common on mountains, where many other life forms (and presumably parasites) might find the going tough. It's probably no accident, either, that notorious asexuals like the bdelloid rotifers and Darwinulid ostracods live in freshwater habitats: dispersal to avoid parasites and found new colonies might be easier in water. And the bdelloids seem to have evolved an additional trick. They can spring Lazarus-like back to life from a completely desiccated state, surviving droughts that might kill off water-borne parasites before they take root. But none of this is easy to prove, and fleetness of foot is clearly no passport to asexuality. Plenty of organisms disperse rapidly yet remain firmly wedded to sex-butterflies, for example. Besides, an ability to escape parasites alone might not be enough. Research into why sex reigns supreme in biology fingers another, more insidious, foe. In theory, each time organisms reproduce they risk passing on random DNA errors to their offspring. This is because the machinery that copies and proofreads DNA isnt perfect. Individually such mutations would be relatively harmless. But collectively they could add up to something more damaging. Indeed Kondrashof, and others argue that if such mutations were allowed to accumulate unchecked in a species' DNA, generation after generation, they might trigger a sudden and catastrophic decline in species fitness. Averting stich a disaster might be one of tile key dividends of sex. By relentlessly shuffling DNA from generation to gelleration, sex ensures that some individuals in a population are born (quite by chance) with very few mutations while others inherit (again, quite by chance) much more than their fair share. The winners in this lottery will go on to replenish the population's gene pool; the losers will fall by the wayside. Unfair? But then biology is like that, and besides, the end justifies the means. The few individuals that are sacrificed and take their mutations with them to the grave mean that the accumulation of mutations in the species as a whole is stopped. "Sex is one way," as Meselson puts it, "to avoid what could be called the entropy death of all life." The catch is that entropy only has a licence to kill species if the random mutation rate is at least one per individual per generation. And for large populations, an additional condition emerges from biologists' calculations; sex can only stop random mutations accumulating in species if the mutations exercise a 'mob mentality". The combined harm of inheriting, say, three or four mutations must exceed the simple sum that whicheach mutation causes separately. Otherwise the losers in the lottery of sex won't die as they surely must. For much of the past decade, there has been scant evidence for any of this, and the parasite theory has taken centre stage. But aspiring asexuals take heed: death by entropy is beginning to look like a credible phenomenon. One new study involves a unicellular algae called Chiamydomomas, which can alternate between sex and cloning. Adan de Visser of the University of Wageningen in the Netherlands and his colleagues compared how mutated Chiamydomonas clones fair following sexual and asexual reproduction. Their findings'support the idea that mutations canas theory demands-wreak proportionately more havoc when inherited in "mobs' than when inherited separately. Other studies showing this are expected to be published later this year.

Sexless prisoners

Meanwhile, at the University of Arizona in 7bcson, molecular biologist Nancy Moran has uncovered further evidence for the mutation theory from symbiotic bacteria trapped inside the cells of aphids, white flies and other insects. The bacterium Buchnera aphidicola, for example, seems to have infected its aphid hosts 100 to 250 million years ago. Since then, it has been confined to a life without sex. By comparing genes from such sexless symbionts with those for their promiscuous free-living relatives, Moran has produced a precise chemical readout of what abstinence does to DNA. The bad news for would-be asexuals is that sexless bacteria do indeed clock up harmful mutations faster than normal. The good news is that they have so far avoided death by entropy. How, nobody knows, but Moran points out that the Buchnera bacteria contain high levels of so-called chaperone molecules.t Free-living cells use chaperonet much as harried executives use therapists-to prevent their internal bits and pieces (proteins in particular) froni falling apart in response to high temperatures and other stresses. Perhaps, speculates Moran, the sexless symbionts have found another use for these chaperones keeping their severely mutated proteins working. Some sexless species have come up with what seems to be an entirely novel way of keeping mutations at bay. During reproduction, they shed or synthesise a new spare copies of genes and chromosomes. Some amoebas and protozoa carry half a dozen or more copies of their genomes, with the precise number changing from generation to generation. Echoes here of sex itself, which involves the amount of DNA doubling when sperm and egg fuse and then halving again when the new individual produces its own sperm or egg cells. Kondrashov, for one, believes that the protozoa may in fact be using a primitive ancestral form of sex to avoid death by entropy.

Genetic gremlins

Meselson has his own master tip on how to survive without sex: rid yourself of transposons. He suspects these flighty chunks of DNA that can "jump" around chromosomes may be the big gest problem of all for creatures lacking sex. Most mutations and DNA copying errors cause little or no damage to genes, he points out-but not transposons. "if you insert a chunk of DNA into a gene, it's a dead gene for sure." Not only that: "'These things are alive in the sense that they can reproduce in your genome and multiply," Keeping the numbers of these genetic gremlins down to safe, levels is the key to why we need sex, Meselson believes. Trouble is, experiments on bacteria suggest transposons may not be so damaging after all. By creating beneficial mutations as well as harmful ones, they might even help some organisms. But then, no one theory in biology's great'Why sex?'debate has yet been refined to the point where it works perfectly or can account for all the facts. Parasites don't always kill their hosts, mutations aren't always a bad thing (without them, after all, we'd still be slime). The overarching question is whether sex is primarily about making sure that good genes spread or that bad ones don't. And here, says Hurst, 'we're squirming our way towards a final conclusion'. Some of us have more need to squirm than others. Human biology is, it's true, wired up for sex and nothing else. That means ditching males isn't yet an option for our own species. In the long term, though, it may be precisely what evolution is inexorably working towards. in humans as in all mammals, sex plainly depends on the Y chromosome, without which there would be no males. The irony is that the Y chromosome itself can reap none of the benefits of sex. All other chromosonies are inherited in pairs, enabling them to exchange genetic material with a partner. But not, alas, the Y chromosome. Confined to a lonely life withotit sex, it is, says Hurst in the same perilous genetic boat asother ancient virgins Indeed accroding to an analysis of Y chromosome sequences, its genes are changing much faster than genes on other human chromosomes. Ominously, it's not yet clear whether the changes being rung on the Y chromosome amount to rapid adaptive evolution or rapid decay. But the fact is that science knows of only a few ancient virgins that have avoided premature extinction.

Are you feeling lucky, guys?