queen of hearts, Attribution: Jamiesrabbits, FlickrProceedings B Darwin Reviews are special reviews published up to once a year. The aim of the Darwin Review is to showcase ideas and/or a field in biological science that is of very high interest to the whole diverse readership of Proceedings B, often being of particular relevance to strategic growth areas, importance to policy makers and/or having a bearing on the public that fund our science.
This year our Darwin review revisits a seminal theory in evolutionary research, Van Vaalen’s Red Queen Hypothesis. 40 years after its initial proposal the Red Queen is still informing research. Here the authors discuss their review and why now was the right time to highlight the Red Queen’s enduring legacy. You can read the full article here. Our previous Darwin review was on evolutionary medicine and can be found here.

Tell us about the Red Queen hypothesis.
The Red Queen hypothesis was proposed over 40 years ago by the late evolutionary biologist Leigh Van Valen. It advanced evolutionary thinking beyond the idea that organisms were merely matched to their physical environment by suggesting that interactions between species (such as between hosts and parasites, predators and prey) would also be important in driving evolutionary change. In essence, the Red Queen hypothesis states that in the battle for resources, species must continuously evolve just to keep up with their enemies, who themselves also evolve in response. The result is that species constantly change but, relative to their enemies, don’t actually get any fitter – like running on an evolutionary treadmill. The name for the theory came from Lewis Carroll’s ‘Through the Looking Glass’ (aka Alice in Wonderland). Alice finds herself in a race with the Red Queen, and despite running as fast as she can, Alice stays in the same place. The Red Queen hypothesis, doubtless partly due to this imaginative metaphor, has become one of the most influential ideas in evolution.

How has the theory influenced evolutionary biology research since its original proposal?
Van Valen was interested in macroevolution, that is speciation and extinction, and used the Red Queen hypothesis to explain the apparently constant rates of extinction observed in the fossil record. And although this pattern has subsequently been challenged, Red Queen thinking is still important in macroevolution in terms of understanding the biological, as opposed to environmental, causes of diversification and extinction. In the 1980s, the utility of the Red Queen concept was rediscovered as a way of explaining the ubiquity of sexual reproduction in nature. The idea starts by considering that hosts and parasites are evolving together. If the hosts are sexual females, they can produce offspring that are genetically diverse and therefore avoid parasite infection. However, if hosts are clonal females, their offspring lack the ability to be as genetically diverse and will be more susceptible to attack by parasites. Thus, coevolution with parasites prevents the clones from taking over and gives sexual species an advantage. Increasingly, biologists think of the Red Queen hypothesis, not only as an explanation for sex, but also as a means of explaining rapid evolutionary change in hosts and their parasites in general. .

What prompted you to write this review?
The adoption of the Red Queen as an explanation for the evolution and widespread maintenance of sex led to a narrowing of the definition of the Red Queen hypothesis. This meant that the far richer perspective of Van Valen’s original conceptual leap was in danger of being lost. To some extent, we wrote the review because we believed it was necessary to reemphasize a broader importance of the Red Queen hypothesis because it offers a powerful way in which to understand natural communities, how they evolve, and how they work. It is an important and useful idea. We were also inspired by the data emerging from new approaches of studying species interactions, including genome sequencing and experimental evolution in the laboratory. These present a more complex and nuanced picture of the effect of species interactions on evolution that is entirely consistent with a Red Queen view of nature.
Additionally, we were aware that much of theory developed to understand how conflicts between species evolve could be usefully applied to understand conflicts within species. A variety of conflicts have been defined in this context: intragenomic conflicts (e.g. over the representation of chromosomes in gametes during meiosis), sexual conflicts (e.g. between males and females over reproductive effort and timing) and parent / offspring conflicts (e.g. over the allocation of resources to progeny). However, the evolutionary dynamics of these conflicts has never formally been synthesized within the Red Queen concept, despite the clear ability for these conflicts to generate the type of ‘running to stay still’ evolutionary dynamics. One of our aims in this review was therefore also to attempt this synthesis.

What does the future hold the red queen hypothesis?
It will certainly be informative to see how useful and explanatory is the incorporation of conflicts within species into the Red Queen framework. Beyond this, we recognise that much of our appreciation of the Red Queen currently comes from studying binary relationships (one parasite in one host). Extensions of this to more realistic scenarios, by incorporating parasites that evolve with a range of hosts, and hosts that evolve with a range of parasites, are therefore needed. How these will affect the speed of the Red Queen needs to be determined. Finally, there has been increasing use of comparative genomics to examine evolutionary dynamics. However, these analyses are limited in that the function of many genes is not known, making it difficult to determine the contribution of the Red Queen. Commonly, for instance, expression patterns indicate that specific genes are involved in male-female interactions, and could therefore be subject to coevolution. However, at the moment, we cannot differentiate the subset of genes that are involved with the male-female interface that are likely to be subject to Red Queen forces from those involved in a variety of other sex-specific physiological functions. We also have incomplete ascertainment of genes at the host-pathogen boundary: we understand host genes that are generically involved in defence much better than those which alter microbial invasion into a cell. We expect the results of comparative genomic analysis of Red Queen type processes to be made sharper as our understanding of gene function improves.

Meet the authors
Michael Brockhurst is Professor of Evolutionary Biology and a 50th Anniversary Chair at the University of York. He uses experimental evolution approaches to study the coevolution of species interactions with a particular focus on bacteria and their viral and genetic parasites. He is interested in the applied consequences of rapid microbial evolution in natural communities especially in clinically important pathogenic microbes.

Greg Hurst is Professor of Evolutionary Biology at the University of Liverpool. His main goal is to determine the ecological and evolutionary importance of heritable symbionts of insects (where symbiont is broadly defined and includes parasitism), and has an interest intragenomic and intra-specific conflicts more generally. His study animals include Drosophila, Nasonia wasps, butterflies and ladybirds, and the symbionts studied are largely microbial.

Kayla King is an Associate Professor at the University of Oxford. Her research explores the ecology and evolution of species interactions to ask fundamental questions about the maintenance of genetic and community-level diversity, sexual reproduction, and rapid evolutionary change. She focuses on interactions between hosts and their parasites as well as their microbiota.

Judith Mank is Professor of Evolutionary and Comparative Biology at University College London. She is interested in the constraints imposed on the genome by sexual conflict, and how selection navigates these restrictions of genome architecture to create intra-specific phenotypic diversity in the form of sexual dimorphism. She works on a range of study organisms, most recently birds, fish and flies.

Steve Paterson is Professor of Evolutionary Biology and a director of The Centre for Genomic Research at the University of Liverpool. He is primarily interested in understanding the forces that shape genetic diversity within host and parasite genomes. New genomic methods that allow us to address this question make it clear how much we owe to the Red Queen for our understanding of genome evolution and of the novel biology yet to be discovered from biotic interactions.

Tracey Chapman is Professor of Evolutionary Biology in the School of Biological Sciences at the University of East Anglia. She is interested in understanding the nature and the evolutionary potential of reproductive interactions between males and females. Such interactions are often subject to sexual conflict and can generate rapid evolutionary change.

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