“It takes all the running you can do, to keep in the same place.” 

The Red Queen, Through the Looking-Glass, Lewis Carroll.

    How did sexual reproduction evolve? How do parasites and their hosts survive together? Why do predators manage to catch their prey only some of the time? To answer  these questions, we journey into the Kingdom of the Red Queen. A realm in the universe of biology that has an answer for all these questions and many more. In its entirety,  the Red Queen Hypothesis states that in any co-evolving environment, each species needs to continually change itself to adapt to environmental changes in order to compete and co-exist with another co-evolving species in the same environment. Confused? 

    Here's a simpler example. Imagine the savannahs of Africa. Sunny. Warm. Beautiful. Dangerous. The lionesses stalk the gazelle. Silently creeping up to the ungulate until the last moment when all hell breaks lose and it ends being a race to the finish. The gazelle is fast and nimble, the lioness more plodding but equally fast. In a scene right out of the Discovery Channel, the lioness finally fells the hapless gazelle and there's food for the pride. The hunt has been going on identically for hundreds of thousands of years, except for one variable. Speed. The gazelle gets a little bit faster to avoid being eaten. The lioness becomes that little bit faster to catch the gazelle. And then the gazelle gets a little faster again. And so on. The arms race of biology.

    Examples of such attempts at biological one-up-manship abound. The African cuckoo finch lays its egg in another bird's nest, and once the cuckoo's egg hatches, the fledgling eliminates competition for food by pushing the other eggs out of the nest. Over time, the victimised birds have evolved a strategy of laying coloured eggs that are easily distinguishable from the cuckoo finch. Right now, the victims have the advantage. For the cuckoo finch to survive, it has to be capable of evolving the ability to compete; potentially by laying similarly coloured eggs that are indistinguishable from that of the victim. 

    The Red Queen has her reach in the many other fields of biology too. One of the biggest questions in evolutionary biology is on the origin of sexual reproduction. Essentially,  males are expensive and worthless. They are simply, a bag of genes. While required for sexual reproduction, males are incapable of producing offspring themselves, which results in something called the “twofold cost of sex” or “the cost of males”. Simply put, in a stable environment, without any external pressures (such as a parasite), selfing (or self-fertilisation, the act of reproduction without the requirement of another individual of a different sex) results in higher numbers of progeny than a species that are out-crossers (require another individual of a different sex, ie male or female). This is because while the out-crossing species requires two parents to produce offspring, the selfing species requires just one parent to produce offspring. 

Thus, over time, the selfing species will produce two times the number of offspring than the out crossing species, and will eventually be the dominant species in the given environment. Given this, why do a number of vertebrates and plant species still exhibit sexual reproduction? It was widely assumed that sexual reproduction; ie the mixing of two different genetic backgrounds would produce a variant of an offspring that could respond better to drastic changes in environmental conditions. This is in contrast to selfing, where offspring would be essentially identical to their “mother” (or hermaphroditic parent). For instance, when a species is challenged by a pathogen, then the out-crossing species, with the inter-mixing of genes would be better capable of producing a variant that was immune to the onslaught of the pathogen. Over time, this variant would survive and reproduce more succesfully than the other variants, and eventually become widespread in this environment. The selfing species however, would produce a variant progeny much slower (because a change has to occur in the parent by mutation, which is rarer) and establishment of this variant would require the replacement of all other non-variant individuals.

     While this makes sense as a thought experiment, it was only recently proved in a truly biological setting. The laboratory.  Researchers at Indiana University used  Caenorhabditis elegans (C elegans), a commonly used laboratory microscopic worm to test for the ability of the worm to shift from  the more common hermaphroditic form of reproduction to sexual reproduction in the presence of the pathogenic bacteria, Serratia marcescens. A normal (wild type) population of C elegans primarily exists in hermaphroditic state, with only 15-20% of all the worms being males (implying about 15% of sexual reproduction in a population). However, once the pathogenic bacteria was added, the proportion of males sky rocketed from 20% to 70% suggesting that presence of the pathogen resulted in “selection” for the out-crossing individuals.

They also showed that increase in prevalence of males was dependent on the ability of the bacteria to evolve. When exposed to bacteria that did not evolve, the proportion of males rose, but dropped back to normal levels of 20%. This is suggestive of the fact that an increase in out crossing would result in potential genetic variants that could be resistant to continual bacterial infection. This interaction is suggestive of the Red Queen effect, wherein the worm had to evolve faster in order to keep pace with the co-evolving bacteria. Once the evolution of the bacteria was stopped, then there was no advantage to the out-crossing worms, and there was a return to hermaphroditic ways.

The researchers further concluded the benefits of sexual reproduction by allowing bacteria to infect worms that were obligate selfers (ie mutated to be capable only of selfing) or obligate crossers (only capable of out crossing). Upon infection with a co-evolving bacteria, the obligate selfers were extinct within 20 generations, but the obligate crossers never went extinct. Thus, the authors concluded that this co-evolution experiment with the worm and its pathogen was direct proof of the Red Queen hypothesis. Out crossing was selected for in the presence of continual environmental change, but the cost of sex was not worth it in a stable environment (non- evolving bacteria or lack of bacteria). 

    This further raises the question of why many vertebrates, such as mammals exhibit out crossing, when many invertebrates, some fish and a few reptiles are either hermaphrodites, can change sex depending on the environmental condition or exhibit parthenogenesis (female birth/virgin birth). This again is related to changing environments. Many obligate selfing or asexually reproducing species are highly restricted to one environment, since they cannot survive if the environment condition changes or a pathogen arrives and changes faster than they can. Out crossing individuals however are capable of evolving to meet the challenge, and therefore more widespread in their distribution and ability to survive. Over evolutionary time, the benefits of survival  and expansion into new pastures far outweigh the numerical benefit that selfing offers, resulting in a fixation of sexual reproduction as the predominant means of producing offspring. 

    The Red Queen hypothesis can be used to answer some other questions as well. The presence of certain inherent proteins in monkeys and humans that can restrict HIV or its relatives (Simian Immunodeficiency Virus; SIV) can also be traced back to the co-evolution of the host (either human or monkey) to that of the virus (SIV). The Red Queen can also be used to explain the development of the immune system. Despite the wide ranging implications of the Red Queen hypothesis, she is not the only contender in the evolutionary battle.

The Red Queen hypothesis was originally used to describe competition between species being the driving factor behind the large number of species we see today. Another hypothesis, known as the Court Jester hypothesis suggests that changes in species may result not due to competition between species, but due to random geological or climate events that act as the driving force behind evolution, and the formation of new species. 

    Finally, the Red Queen can also be used to explain certain observations in the real world. Would the Americans and Soviet spent so much on weapon development if the other was absent in the global battlefield? Would so many tech companies care to develop their tech toys if it were not for Apple's forays into the iPhone and iPad?

The world of evolution need not be restricted to studying fossils or our present biodiveristy. A change in our thinking, the decisions we make, can all be linked in some aspect, to the basic framework of evolution. And many of these choices fall into the hands of the Red Queen, who suggests that the constant battle of survival, between animals, technology or arms is responsible for the world we live in today. 

    The Red Queen is not dead. Long live the Red Queen. 


References:

 1. Spottiswoode and Stevens. How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defenses. 2011. Proceedings of the Royal Society B: 1-7. 
2. Feigel et al. Sex is always well worth its two-fold cost. 2009. PloS One. 
3. Brockhurst, MA. Sex, death and the Red Queen. 2011. Science :166-167.
 4. Morran T et al. Running with the Red Queen. Host-Parasite Coevolution selects for Biparental Sex. 2011. Science: 216-218. 
5. Barnosky, A.  Distinguishing The Effects Of The Red Queen And Court Jester On Miocene Mammal Evolution In The Northern Rocky Mountains. 2001.  Journal of Vertebrate _Paleontology: 172–185.