Sex & the Reign of the Red Queen

Why sexual species beat clones every time.

Tenniel_red_queen_with_alice

“Now, here, you see, it takes all the running you can do to keep in the same place.”

From a simple reproductive perspective, males are not a good investment. With apologies to my Y chromosome-bearing readers, let me explain. Consider for a moment a population of clones. Let’s go with lizards, since this actually occurs in lizards. So we have our population of lizard clones. They are all female, and are all able to reproduce, leading to twice the potential for creating more individuals as we see in a species that reproduces sexually, in which only 50% of the members can bear young. Males require all the same resources to survive to maturity, but cannot directly produce young. From this viewpoint alone, the population of clones should out-compete a bunch of sexually-reproducing lizards every time. Greater growth potential. What’s more, the clonal lizards can better exploit a well-adapted set of genes (a “genotype”); if one of them is well-suited to survive in its environment, they all are.

Now consider a parasite that preys upon our hypothetical lizards. The parasites themselves have different genotypes, and a given parasite genotype can attack certain host (i.e. lizard) genotypes, like keys that fit certain locks. Over time, they will evolve to be able to attack the most common host genotype, because that results in their best chance of survival. If there’s an abundance of host type A, but not much B or C, then more A-type parasites will succeed in reproducing, and over time, there will be more A-type parasites overall. This is called a selection pressure, in favour of A-type parasites. In a population of clones, however, there is only one genotype, and once the parasites have evolved to specialise in attacking it, the clones have met their match. They are all equally vulnerable.

The sexual species, however, presents a moving target. This is where males become absolutely worth the resources it takes to create and maintain their existence (See? No hard feelings). Each time a sexual species mates, its genes are shuffled and recombined in novel ways. There are both common and rare genotypes in a sexual population. The parasite population will evolve to be able to attack the most common genotype, as they do with the clones, but in this case, it will be a far smaller portion of the total host population. And as soon as that particular genotype starts to die off and become less common, a new genotype, once rare (and now highly successful due to its current resistance to parasites), will fill the vacuum and become the new ‘most common’ genotype. And so on, over generations and generations.

Both species, parasite and host, must constantly evolve simply to maintain the status quo. This is where the Red Queen hypothesis gets its name: in Wonderland, the Red Queen tells Alice, “here, you see, it takes all the running you can do to keep in the same place.” For many years, evolution was thought of as a journey with an endpoint: species would evolve until they were optimally adapted to their environment, and then stay that way until the environment changed in some fashion. If this was the case, however, we would expect that a given species would be less likely to go extinct the longer it had existed, because it would be better and better adapted over time. And yet, the evidence didn’t seem to bear this prediction out. The probability of extinction seemed to stay the same regardless of the species’ age. We now know that this is because the primary driver of evolution isn’t the environment, but competition between species. And that’s a game you can lose at any time.

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Passionflower. Photo by Yone Moreno on Wikimedia Commons.

Now the parasite attacking the lizards was just a (very plausible) hypothetical scenario, but there are many interesting cases of the Red Queen at work in nature. And it’s not all subtly shifting genotypes, either; sometimes it’s a full on arms race. Behold the passionflower. In the time of the dinosaurs, passionflowers developed a mutually beneficial pollinator relationship with longwing butterflies. The flowers got pollinated, the butterflies got nectar. But then, over time, the butterflies began to lay their eggs on the vines’ leaves. Once the eggs hatched, the young would devour the leaves, leaving the plant much the worse for wear. In response, the passionflowers evolved to produce cyanide in their leaves, poisoning the butterfly larvae. The butterflies then turned the situation to their advantage by evolving the ability to not only eat the poisonous leaves, but to sequester the cyanide in their bodies and use it to themselves become poisonous to their predators, such as birds. The plants’ next strategy was to mimic the butterflies’ eggs. Longwing butterflies will not lay their eggs on a leaf which is already holding eggs, so the passionflowers evolved nectar glands of the same size and shape as a butterfly egg. After aeons of this back and forth, the butterflies are currently laying their eggs on the tendrils of the passionflower vines rather than the leaves, and we might expect that passionflowers will next develop tendrils which appear to have butterfly eggs on them. These sorts of endless, millennia-spanning arms races are common in nature. Check out my article on cuckoos for a much more murderous example.

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Egg-like glands at the base of the passionflower leaf (the white dots on my index finger).

Had the passionflowers in this example been a clonal species, they wouldn’t likely have stood a chance. Innovations such as higher-than-average levels of cyanide or slightly more bulbous nectar glands upon which defences can be built come from uncommon genotypes. Uncommon genotypes produced by the shuffling of genes that occurs in every generation in sexual species.

And that, kids, is why sex is such as fantastic innovation. (Right?) Every time an illness goes through your workplace, and everybody seems to get it but you, you’ve probably got the Red Queen (and your uncommon genotype) to thank.

 

Sources

  • Brockhurst et al. (2014) Proc. R. Soc. B 281: 20141382.
  • Lively (2010) Journal of Heredity 101 (supple.): S13-S20 [See this paper for a very interesting full explanation of this links between the Red Queen hypothesis and the story by Lewis Carroll.]
  • Vanderplank, John. “Passion Flowers, 2nd Ed.” Cambridge: MIT Press, 1996.

*The illustration at the top of the page is by Sir John Tenniel for Lewis Carroll’s “Through the Looking Glass,” and is now in the public domain.