Realised hypothetical phenotypes and the adaptive value of Batesian mimicry

Many animals, such as venomous snakes or stinging wasps, advertise to potential predators that they are well defended by displaying bright, bold colour patterns. Other animals, known as "mimics", have evolved to deceive predators by displaying patterns similar to the dangerous "models", despite being harmless. Studying the evolution of mimicry has the potential to tell us much about how natural selection leads to adaptation in wild animals.

Among mimics, we see many prominent and beautiful examples of the extreme adaptations that evolution can produce. However, some mimics, including many hoverflies that mimic wasps, only approximately resemble their model. We expect natural selection to favour the most convincing mimics, because less good ones ought to be recognised and picked off by predators: so why are some mimics inaccurate? Perhaps predators (such as birds) do not pay attention to all aspects of the prey's appearance, so the mimic does not have to be accurate in every way. Birds might avoid all prey that are roughly similar to a particularly nasty model, so beyond a certain point, further accuracy is unnecessary. Alternatively, the best chances of survival may gained by mimics which approximately resemble several nasty model species, rather than those which are perfect mimics of one particular model.

To test these ideas, we need to know not only how successful existing mimics are, but also the performance of alternative mimics with different combinations of features to the existing ones. Would a more accurate mimic survive better? What if it were perfect except for its colour? This is an example of a more general problem in evolutionary biology, of predicting how non-existent, but theoretically plausible, organisms might perform in comparison to those that we observe in nature.

To explore the evolutionary potential of mimics, our project brings together recently-developed technologies in a way never exploited before by biologists. First, we will photograph hoverflies and wasps from multiple angles and assemble 3D digital representations. We will then create new "morphed" images of plausible, but imaginary, intermediates between hoverflies and wasps which vary in similarity to the wasps. Thirdly, we will use 3D printing to create models of these intermediates (as well as the "real" insects) that are realistic in terms of their size, colour, pattern and shape. Lastly, we will measure the "survival" of these 3D models in a variety of experiments.

We will test the response of predators by training birds to "attack" models of hoverflies, but avoid those of wasps, in order to gain food rewards. Having learnt that distinction, the birds will then be tested for how they behave towards 3D models of intermediate appearance. The longer the birds hesitate before attacking, the more effective is the mimicry, because in the wild such delays would give the insect an opportunity to escape. We will look at predator behaviour both in the wild, where natural communities of birds with varying levels of experience are foraging for food, and in the laboratory, where we can control the experiences of each individual and watch how they learn. We will also repeat the experiments using praying mantises in place of birds, to investigate whether insect predators judge mimicry differently.

Our project addresses a long-standing biological question about the evolution of inaccurate mimicry, but will also provide broader insights into evolutionary processes. What is it about existing species that mean they survived when others either did not survive, or never evolved in the first place? This in turn allows us to understand how evolution produced the combinations of characteristics of existing species, and to predict the direction that evolution might take in the future. Our novel method will provide a framework for other evolutionary biologists to explore similar questions in a wide range of different organisms.

Our proposed research is "Discovery Science": the primary motivation is curiosity regarding fundamental questions about the way organisms evolve. As with all such "blue skies" research, it has the potential for wide-ranging economic and societal impact in the future in ways that are difficult to predict, but which are no less important as a result.

In addition to this, because we are studying a highly accessible and intuitive example of evolution by natural selection (Batesian mimicry), our project provides the perfect opportunity for outreach and increasing the public understanding of science (especially evolution). We will run experiments in schools to teach children about evolutionary processes, and enthuse them about scientific experiments. Replicating our laboratory experiments in the school environment will increase interest and excitement from the learners, because they can see that they are participating in ongoing research with an uncertain outcome. Crucially, our partner schools are part of the "Widening Participation" scheme at the University of Nottingham, which aims to stimulate interest in university education amongst pupils from disadvantaged backgrounds. Our colleagues in the School of Life Sciences have shown that getting these children actively involved in novel scientific research is especially effective at both engendering enthusiasm for science and improving subject knowledge [1].

Batesian mimicry is an ideal case study for teaching about evolution, as the variation in question is on show in a visually striking way, and the principles behind the fitness benefits that mimicry brings (increased protection through deceiving predators) are easily understood. FG, TR and CT have all had great success in the past in using Batesian mimicry in teaching sessions for school children (of a range of ages). For example, CT has presented practical sessions based on the topic of mimicry at the Sutton Trust Summer School, which is aimed at increasing interest and enthusiasm for higher education among year 12 students from state-maintained schools. These sessions received excellent feedback, indicating that the attendees were more likely to consider studying a similar topic at university as a result. TR has run an experiment in primary schools, in which children play the role of a "predator" in a computer game, to test hypotheses about mimicry [2]. This experiment was embedded in a class activity about the principles of evolution, which stimulated fascinating debate amongst pupils. We plan to create a modified version of the above computer game for use during school sessions, and will also publicise the game more widely in order to engage and educate the general public in the topic of evolution.

1. Devonshire, I.M., et al. (2014). PLoS ONE, 9: e103640.
2. Morris, R. & Reader, T. (in prep) [Available online at http://ecology.nottingham.ac.uk/NERC]