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Saturday, February 26, 2011

Sex and the Red Queen

"Well, in our country," said Alice, still panting a little, "you'd generally get to somewhere else — if you run very fast for a long time, as we've been doing."

"A slow sort of country!" said the Queen. "Now, here, you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!"
-- Lewis Carroll, "Through the Looking Glass and What Alice Found There"

Would you believe that passage inspired one of the most important theories in modern biology?

A question (some would say THE question) that continues to produce one of the most heated debates among scientists is one of the most fundamental: Why is there sex?

Can you believe that we (when I say "we" I mean all of modern science, with our hoity-toity technology and molecular genetics) have not answered this question yet?

You may be thinking: "Well duh, you need sex to reproduce!"  You may, but not everyone does.  Bacteria don't, and there are way more of them than us.  Certain animals don't!  Entire generations of aphids reproduce asexually.  In some animals reproduction is always asexual, such as the bdelloid rotifers that have been cloning themselves for millions of generations.  Among fish, reptiles and birds, some species are known to avoid sex when reproducing.  Everyone lays eggs, and as such everyone is female.

If you think about it, the question shouldn't be "Why sex?"  It should be: "Why males?"

In the 1970s a clever biologist named John Maynard Smith asked this question by playing a little game.  His game went like this: suppose there exists a population in which some individuals reproduce sexually and others reproduce asexually.  He imagined a founding population with three individuals: a male sexual, a female sexual, and a female asexual and assumed that both females could produce two eggs each.  The male and female sexuals would need to get jiggy and produce a son and a daughter from their two eggs, while the female asexual made a couple of daughters from hers.

Already the asexuals went from 1/3 of the population (sex male: sex female: asex female) to 1/2 of the population (sex son: sex daughter: asex daughter: asex daughter).  Playing the game for just one more generation puts the asexuals ahead!  The sexual son and daughter make a couple of offspring (a boy and a girl), but the two asexual daughters make two female offspring apiece for a total of four asex granddaughters!  Hence after two rounds of mating asexuals have the numerical advantage of 2/3 of the population. And that advantage increases with each additional generation.

Sex is a losing strategy in a pure numbers game because males don't make eggs.

Now that fundamental question doesn't seem quite as lame, huh?  So .. Why males?!?

The answer must be that the numbers game does not give asexuals an advantage in most species of plants and animals.

Cue the heated debate.  The scientific literature is full of theories, many of them heavy on the math, many of them heavy on the genetics, but two of the main contenders are fairly intuitive.

The first contending theory, credited to another clever biologist named Alexy Kondrashov, is that sex evolved because it made possible the elimination of bad mutations from sexual populations while asexual populations accumulated more and more harmful mutations.  In sex we shuffle up our chromosomes and only pass on half to each offspring.  Because each offspring is a random half-mix of each parent there is a good chance it might luck out and NOT inherit a particular bad mutation.  Unfortunately some of its brothers or sisters probably will, but natural selection takes them -- and their bad mutations -- out of the gene pool.  Asexuals, however, pass on bad mutations to ALL their offspring, some of whom will produce even more new and different bad mutations in addition.  The gene pool gets more and more polluted over time and puts asexuals at a disadvantage in the game.

The second contending theory, credited to yet another of those clever biologists named Leigh Van Valen, is all about the Red Queen.  What if, in an evolutionary sense, it takes all the running you can do to stay in the same place?

In this version of the game, sexual shuffling results in all sorts of new combinations of chromosomes each generation.  Let's say a particular combination fell into evolutionary disfavor in the past, but then the environment changed in a way that favors it once again.  No problem!  A little sex and we get that combination back!  But asexuals are out of luck because their offspring still have the SAME combinations their parents had.  If natural selection removes a particular asexual combination from the population it never comes back.

Suppose natural selection kept changing directions, back and forth.  It would take all the running (in an evolutionary sense) that a population could do to keep in the same place -- the place of non-extinction!
But does it really work that way?  Why would natural selection keep changing directions?

The work of Curtis Lively (the last clever biologist I will mention today) and his colleagues at Indiana University have put the Red Queen to the test by examining a snail that plays John Maynard Smith's game.  Some populations of Potamopyrgus antipodarum are comprised ONLY of asexual females.  In other populations, however, there are a mix of sexual males, sexual females, and asexual females.

Why don't asexuals win Maynard Smith's game in these particular populations?  The answer may seem surprising: some populations get worms!

Various species of trematode parasites infect Potamopyrgus antipodarum and cause them to become infertile.  Infertility, as far as natural selection is concerned, is the same as death.  You can't pass on your genes to the next generation.

The worms are best able to infect snails with genetic combinations that are least resistant to infection.  What happens to those combinations in a pond full of trematodes?  They don't get passed on.  The remaining snails reproduce and fill out the next generation.  Common snail genotypes become rare and rare genotypes become common.  Any versions of the worm that can infect the new snail population now have the advantage.  The new genetic combination in the snails does not enjoy its supremacy for long.  This is called frequency-dependent natural selection: the fitness of a genotype depends on its frequency: high fitness when rare, low fitness when common.

Remember the snail genotype that was eliminated by trematode infections in the first round?  When the trematode population changes direction, wouldn't it be great for the snails to get that genotype back?  They can -- if they can have sex!  Asexuals, alas, are out of luck.

Dr. Lively and his colleagues found that trematode parasites are most common in ponds with sexual snails -- the more parasites, the more males.  They also found that particular snail genotypes rose and fell in frequency over time in ponds with parasites.  And that parasites in ponds were best at infecting whatever snail genotype was most common at the time.

All of these outcomes support a Red Queen hypothesis that snails are evolving quickly (in terms of genetic changes over time) but staying in the same place (disfavored genotypes later become favored and then disfavored all over again).

The Red Queen hypothesis may or may not turn out to be the ultimate explanation for sex in all species that practice it, but in Potamopyrgus antipodarum, at least, it can keep them one step ahead of their asexual competitors.

Time to quit writing for now -- I'm late for a very important date.

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