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Friday, June 6, 2008

The Weird Sisters

They just keep getting weirder. The “they” I’m referring to are the bdelloid rotifers — small transparent animals that live in damp places such as puddles, or patches of moss. Among evolutionists, these animals have something of a cult following, because they have a lifestyle that is not supposed to exist. As far as anyone can tell, the bdelloid rotifers are ancient asexuals: they appear to have been living entirely without sex for more than 85 million years. And each time we learn more details of their lifestyle, the wackier it becomes.

Evolving to live without sex is easy; all sorts of organisms do it the whole time. For example: aphids, weevils, snails, water fleas, nematode worms, scorpions, even the occasional lizard, have all been known to evolve asexuality. Instead of reproducing via eggs and sperm, asexuals can reproduce in any number of ways. For instance, some bud off a piece of themselves; the piece grows into a whole new animal. The bdelloids, like many other asexuals, reproduce by means of eggs that don’t need to be fertilized.

No, evolving asexuality isn’t the hard part. The hard part is making an evolutionary success of it.

In the short-term, asexuals seem to have an advantage: they don’t have to waste time finding and seducing mates, but can just get on with reproducing. Not having to find a mate makes it easy for asexuals to live in transient habitats, such as puddles, for it doesn’t matter if they never encounter anyone else. Moreover, because asexuals only have daughters, their populations can grow rapidly. In a sexual population such as humans, females must have, on average, two children for the population to remain the same size. In an asexual population, females only need to have one. If each female has two, the population grows. Sex, in other words, is expensive.

Yet if you look at the great tree of life, asexual groups tend to be out on the twigs: there are no great branches of the tree that contain only asexuals. In other words, no one can point to a big group, such as birds or fish, or even snails, and say, “That’s a group composed only of asexuals.” What this means is that asexuality evolves often, but rarely persists for long: asexuals typically go extinct soon after they appear.

The swift extinction of asexuals, and the absence of big asexual groups, suggests that sex is essential for long-term evolutionary success: giving up sex is a Bad Idea, a kind of evolutionary suicide.

Exactly why this is so remains unclear. But it’s thought to have something to do with the fact that sex generates new gene combinations. Whereas a sexual creature like you or me inherits a unique mix of genes from our parents, asexuals are lumbered with the same set of genes their mother had. For an asexual, then, the only source of genetic novelty is mutation. (Mutations and sex are both sources of genetic variation, but they work differently. Mutations — accidental changes to DNA — are the ultimate source of genetic novelty. However, mutations tend to be harmful more often than they are helpful: they tend to disrupt genes that are already working. Sex, in contrast, takes pre-existing genetic variation and shuffles it, generating new gene combinations.)

Which brings me to the bdelloids. These animals are the great exception: a group of more than 450 species from which sex is entirely absent. How are they managing to flourish despite this epic period of abstinence? For they do flourish: bdelloids are everywhere. Go outside, collect some damp moss, and stick it under the microscope, and the odds are you’ll find some. You can even find them in Antarctica.

One possibility is that they are having sex after all, just very secretly. Certainly, other supposed ancient asexuals turned out to be having sex on the sly. For instance one group of aphids that were thought to be ancient asexuals turned out to be producing males. And genetic evidence has revealed sex in several groups, such as the Placazoa (small animals that live in the sea), that have never actually been seen doing it.

But genetic evidence suggests that the bdelloids are not having conventional sex: their genomes show no sign of it. Instead, they seem to be getting up to something else entirely.

It now looks as though the bdelloids do acquire new genes from time to time — that mutation isn’t their only source of genetic novelty. Yet their means of getting new genes is unlike anything previously known for an animal. Namely: they seem to pick up genes from the environment, and add them into their genomes.

The latest analysis of bdelloid genomes shows that the animals don’t just have rotifer genes. They also have dozens of genes from bacteria, fungi, and plants. For instance, the genome of the bdelloid rotifer Adineta vaga contains genes that bacteria use for making components of their cell walls. (What the rotifer is using them for is unclear.) Some of the other genes the animal has acquired are known only from a few groups of bacteria and fungi.

Which is seriously weird. Horizontal gene transfer — the technical term for when genes move sideways between distantly-related species — is common among bacteria, but extremely rare in animals. The likely reason for the difference is that bacteria have only one cell, and their genes are not sequestered in a cell nucleus, so adding a new piece of DNA here or there is easy. Animals, in contrast, not only keep their genes away from the rest of the cell, in a cell nucleus. They also have specialized sex cells — eggs and sperm. In order for a gene from a fungus to be permanently added to, say, the human genome, it must somehow get into the sex cells.

No one knows how the bdelloids pick up these genes. One idea is that it may be due to another oddity of their lifestyle: their ability to dry up and blow away. When the piece of moss they are living in dries up, these animals often dry up, too. It’s a state of suspended animation — add water and, all being well, they come back to life as frisky, or even friskier, than before. (This isn’t unique to bdelloids — some other small animals have evolved to endure desiccation. But most of these others can only do it at particular stages of their lives. The bdelloids can do it at any time. They can also — probably as a consequence of their desiccation abilities — survive high levels of radiation. Much higher than other animals can.) During the drying and rehydration, cell membranes may become disrupted, and their DNA fragmented. Perhaps all this makes it easier for stray bits of foreign DNA to get into the cells that will become eggs.

Some of the bacterial genes were clearly acquired a long time ago. We know this because they have evolved features that bacterial genes lack. Which suggests that getting new genes this way may be rather rare — the sort of thing that happens maybe once every five hundred thousand years or so. All the same, the occasional acquisition of foreign genes may have helped the bdelloids to their profoundly unorthodox success.

But personally, I’m glad that making a go of chastity is so difficult. For the real lesson from these weird sisters is that, for most of us, it’s far better to have sex.

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NOTES:

The ease of evolving asexuality, and the possible advantages of sex, have been much discussed; see, for example, Bell, G. 1982. “The Masterpiece of Nature: The Evolution and Genetics of Sexuality.” University of California Press. For a non-technical account, see chapter 13 of my book, “Dr. Tatiana’s Sex Advice to All Creation.” Metropolitan Books.

For the number of bdelloid species, see Segers, H. 2007. “Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy, and distribution.” Zootaxa 1564: 1-104. For bdelloids in Antarctica, see Izaguirre, I., Allende, L. and Marinone, M. C. 2003. “Comparative study of the planktonic communities of three lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula).” Journal of Plankton Research 25: 1079-1097.

For how genetics gives clues to sexual or asexual lifestyles, and for examples of “asexuals” engaging in sex on the sly, see Normark, B. B., Judson, O. P. and Moran, N. A. 2003. “Genomic signatures of ancient asexual lineages.” Biological Journal of the Linnean Society 79: 69-84. For the detection of sex in Placozoa, see Signorovitch, A. Y., Dellaporta, S. L. and Buss, L. W. 2005. “Molecular signatures for sex in the Placozoa.” Proceedings of the National Academy of Sciences 102: 15518-15522.

For genetic evidence of the asexuality of bdelloids, see Mark Welch D. and Meselson M. 2000. “Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange.” Science 288:1211-1215; Arkhipova, I. and Meselson, M. 2000. “Transposable elements in sexual and ancient asexual taxa.” Proceedings of the National Academy of Sciences 97: 14473-14477; and Barraclough, T. G., Fontaneto, D., Ricci, C. and Herniou, E. A. 2007. “Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers.” Molecular Biology and Evolution 24: 1952-1962.

For horizontal gene transfer in bdelloids (including the hypothesis that their lifestyle somehow facilitates it), see Gladyshev, E. A., Meselson, M. and Arkhipova, I. R. 2008. “Massive horizontal gene transfer in bdelloid rotifers.” Science 320: 1210-1213. For their ability to dry up and blow away, see Ricci, C. N. 1987. “Ecology of bdelloids: how to be successful.” Hydrobiologia 147:117-127. For their resistance to radiation, see Gladyshev, E. and Meselson, M. 2008. “Extreme resistance of bdelloid rotifers to ionizing radiation.” Proceedings of the National Academy of Sciences 105: 5139-5144.

Many thanks to Dan Haydon and Jonathan Swire for insights, comments and suggestions.

Original here

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