Alice’s Adventures in Parasitsm: Sex and the Red Queen Hypothesis

Everyone who has read Through the Looking Glass knows who the Red Queen is, she’s often regarded as the antagonist of the story as she is the piece directly opposing Alice (the White Queen) and is the source of some general “mischief” throughout the story. However, I believe many people misinterpret her character, she’s not vicious or half-mad like the Queen of Hearts (who the Red Queen is often confused with). In fact, she helps Alice throughout the story by explaining the rules of the game. If anything her character is ambiguous, static, and is simply ‘playing the game’. This is another, often overlooked, reason why the Red Queen is the perfect symbolism for natural selection. Natural selection is often regarded as cruel and systematic, when in reality it is merely a random force of nature that all organisms agree to when joining the race of life and often results in modification that can improve a species.


Another scientist also saw the character of the Red Queen as a perfect symbol for his ground breaking evolutionary hypothesis. In 1973 Leigh Van Valen first coined the term ‘Red Queen Hypothesis’ to explain how coevolved organisms had to evolve constantly to keep up with their counterpart In Through the Looking Glass the Red Queen claims that “it takes all the running you can do, to keep in the same place”  this general sentiment is mirrored in this evolutionary principle, species must evolve (run) in order to remain extant (running in place). Seven years later a parasitologist was the first to take this theory a step further and claim that the Red Queen Hypothesis explained why sexual selection evolved, a dilemma that had been puzzling scientists for years. In his paper Hamilton used a mathematical model to prove that when two populations (only varying in reproduction strategy) both face high intensity natural selection (the kind that pathogens and parasites often create) the population that utilizes sexual selection will have an evolutionary advantage over the other This idea that sexual reproduction allowed hosts to run quick enough to keep up with parasites (that have quicker reproduction rates and faster evolution) became the cornerstone of the modern Red Queen Hypothesis.

This correlation between sexual reproduction and survival makes perfect sense. Remember, sexual reproduction produces genetically diverse progeny with different phenotypes and genotypes. Asexual reproduction results in identical clones and low genetic diversity. When fighting a war with a parasite or pathogen a species would most likely prefer to try every possible genetic combination instead of the same design over and over again. Think about it, if you were in the middle of a zombie apocalypse and you had to choose between a bunker with a never ending supply of flame throwers (which the zombies may eventually become immune to), or a bunker full of different types of weapons, which bunker would you choose? Many experiments have determined that those who pick diversity almost always win the war.


Let me try to explain this hypothesis in the context of something we can all understand, the 1979 movie ‘Alien’. At the risk of getting too nerdy the ‘Xenomorph’ is a fictional alien parasite which hops aboard a spaceship full of humans and begins to use the crew as its own personal incubator. In this example the Xenomorphs (at whatever life stage) is the Red Queen, it is constantly evolving at a quick rate and is able to effectively kill most humans. Ellen Ripley is a human that constantly escapes the parasite (perhaps because of an ‘alien avoidance’ gene, or extremely muscular legs) whereas all of the other humans the parasite encounters die. Thus as long as Ellen Ripley survive the species will too, and hopefully she can pass on whatever trait helps her succeed to her offspring. However, this genetic diversity that has allowed for this heroine to escape was only made possible by sexual reproduction, and has given humans the ability to “keep up” with the parasite.


So, who has the advantage in this constant arms race between parasites and hosts? Parasites have a leg up on the competition mostly due to their ability to produce massive amounts of offspring and their quick generation time. For example, adult schistosomes lay thousands of eggs on a regular basis making their populations incredibly large. They also have very short life spans before reproduction, most parasites can complete their transition from egg to adult form in weeks if they have the right hosts. Hosts on the other hand typically have smaller population sizes, have less offspring, and take years to reach sexual maturity. This allows the parasites to come up with new phenotypes and genotypes much faster than the host which enables them to always stay one step ahead. 


So, if parasites have all of these advantages, how do hosts keep up in this constant evolutionary race? There are a ton of mechanisms hosts have evolved to allow them to keep pace with parasites but the three main categories of anti-parasite behaviors are: avoidance, evasion, and removal. At the American Society of Parasitologists 2015 conference there was a talk given by Dr. Janet Koprivnikar which outlined her research in parasite avoidance in frogs. Her lab has observed amphibians routinely choosing to stay out of parasite infested waters by placing a rock in the organism’s enclosure that they can crawl onto. Interestingly, when the water is not infected with parasites the frog maintains ‘normal’ behavior and doesn’t practice water avoidance, suggesting that the host has evolved a mechanism to recognize and avoid infected waters.  The lab has also witnessed tadpoles (who are restrained to aquatic life) increasing their physical activity in an attempt to get evade infectious stages of parasites. The Koprivnikar lab suggests that these avoidance and evasion strategies are instinctual and a product of a long coevolution between amphibian and trematode.

These behaviors, which have been observed in many species besides amphibians, help a host protect themselves from infection in the first place. However, what can a host do when infection has already occurred? That’s when immunological defense and the removal of parasites comes in. An example of this host defense strategy comes from my own research into the relationship between the Helisoma trivolvis immune system and the Ribeiroia ondatrae. The mollusk immune system mostly relies on freely circulating immune cells called hemocytes, there are two classes of hemocytes: granulocytes and hyalinocytes which are responsible for the detection and destruction of pathogens. Ribeiroia ondatrae in particular is a parasite that Helisoma trivolvis has had a long evolutionary history with, thus the hyalinocytes (the cells responsible for detection) are constantly evolving to more accurately recognize the parasite despite the parasite’s attempts at remaining undetected due to a carbohydrate coat. The granulocytes (the cells responsible for phagocytosing the pathogenic cells) are constantly evolving to better respond to hyalinocytes warnings and eliminate the enemy.

If you’re still having a hard time believing in the Red Queen Hypothesis let me present you with some real life scientific evidence. Dr. Kraaijeveld set up an experiment to test the Red Queen hypothesis using two species of fruit flies (as the host) and wasps (as the parasite). He first allowed the wasps to use the D. subobscura species of fruit fly as their host before switching them suddenly to the D. melanogaster species. 19 of the 20 D. melanogaster individuals survived the attack by mounting an immune defense against the wasp larvae. Dr. Kraaijeveld took this D. melanogaster survivor and used it in breeding a F1 generation while continuing to expose the wasps to D. subobscura individuals, he once again exposed the wasp to D. melanogaster and more and more individuals were able to survive. By allowing the D. melanogaster individuals to evolve and adapt to parasitism, but stunting the parasitic wasps Dr. Kraaijeveld proved the co-evolution via exposure was essential to not only the hosts survival, but also that of the parasite, thus confirming the main tenant of the Red Queen hypothesis.

Another study which helps support the Red Queen hypothesis came from Dr. Curt Lively in 1987 when he observed that more male Potamopyrgus antipodarum (a marker of sexual reproduction) live in water with high parasite intensity than water with low parasite intensity. In fact, sexual reproduction directly correlated with parasite intensity. This study, along with many others carried out by Lively through the years, directly support the Red Queen Hypothesis. Potamopyrgus antipodarum populations, much like Alice, must run as fast as they can (by using sexual reproduction) in order to keep up with the parasite (the Red Queen).


  1. Van Valen, L. (1973). A new evolutionary law.Evolutionary theory1, 1-30.
  2. Carroll, L., Haughton, H., & Carroll, L. (2009). Alice’s adventures in Wonderland; and, Through the looking-glass and What Alice found there. New York: Penguin Classics.
  3. Hamilton, W. D. (1980). Sex versus non-sex versus parasite.Oikos, 282-290.
  4. Koprivnikar, J., J. C. Redfern, and H.M. Mazier. (2014) Variation in anti-parasite behaviour and infection among amphibian host species. Oecologia 174: 1179-1185.
  5. Kraaijeveld, A. R., & Godfray, H. C. J. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.Nature,389(6648), 278-280.
  6. Lively, C. M. (1987). Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature, 328(6130), 519-521.

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