A comparative analysis of the evolution of imperfect mimicry

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There are lots of ways in which animals and plants evolve to look like something else in order to gain an advantage. The stone flounder, Kareius bicoloratus, can change its colour in order to blend in with the sea floor. What looks at first glance like an ant is actually a spider, Myrmarachne japonica. The genus name literally means “ant-spider”: “myrm-“=”ant” and “-arachne”=”spider”. A classic example of mimicry is the genus of moths called Hemeroplanes. The caterpillars of these moths have evolved a startling similarity to snakes which they use (we presume) to deter bird predators. The “head” of the snake is actually the tail of the caterpillar, which is inflated when the animal is alarmed. The tawny frogmouth, an Australian bird which is more closely related to the nightjars than the owls that it resembles, rests on dead trees during the day. The patterning of the bird’s plumage helps camouflage the animal against the tree bark. All of these examples exhibit fairly extraordinary similarities to whatever they are trying to match, demonstrating the capacity of natural selection to produce near-perfect mimics. However, there are many instances where this “mimetic fidelity” falls far short of perfection and a good example of this is the range of mimetic fidelities that occur within the hover flies (Diptera: Syrphidae). Hover flies are a group of “true flies” (order Diptera) so they are related to midges and mosquitoes. The adults mostly feed on nectar and pollen, while the larvae feed on a range of foods (including aphids, and they are recognised as a useful biocontrol agent for these crop pests). Imperfect mimicry in nature Of primary interest to evolutionary biologists, however, is their strong similarity (in some cases, at least) to stinging wasps and bees. However, not all hoverflies are excellent mimics, so the big question is: if natural selection can produce excellent mimics why doesn’t it always do so? This is the puzzle of imperfect mimicry, and there have been a number of hypotheses to explain it: Eye of the beholder hypothesis – Some people have proposed that the hover flies are all good mimics but they only appear poor within the context of human vision. If a bird was looking at these hover flies, it would see all good mimics. Multi-model hypothesis – Perhaps the species are not trying to resemble one wasp, but a number of different wasp species? By not resembling any one species, but partially resembling many, a hover fly would be imperfectly mimetic but still gain benefits through many mimetic associations. Kin selection hypothesis – This hypothesis is a little more complex. If you have a group of wasps and a group of hover flies that are perfectly mimicking those wasps, a predator will attack everything because it cannot differentiate. It has to eat, and a certain proportion of the time it will come across a tasty hover fly (in between being stung by nasty wasps). This means that there is actually no benefit from mimicry at all! However, if some of the hover flies are not perfect mimics, the predator can distinguish hover flies from wasps and so will eat the worst mimics while the best mimics survive. This suggests that there will be an equilibrium resemblance that is close to perfection without ever reaching it. Constraints hypothesis – Maybe there is some other pressure that is pushing back against selection for mimetic perfection? A possible candidate might be thermoregulation, as the patterns of black colouration on the hover flies will affect the amount of heat that is absorbed from the sun. Perhaps this heat absorption is more important than the avoidance of predation, and so colour patterns move away from those that most resemble wasps. Relaxed selection hypothesis – Finally, some scientists have predicted that the intensity of selection might be reduced closer to mimetic perfection and that this might happen earlier in some species rather than others. What we did to test them So how do we test these hypotheses? We used the “comparative method”, which involves looking at many species and comparing their traits in the context of their evolutionary relationships. We asked 21 human volunteers to rate 38 species according to how closely they resembled a wasp, a honey bee or a bumble bee. We then measured specimens of those species (hover flies, wasps and bees) to calculate differences in their shape and size. This gave us two measures of similarity: human rankings and measurements. We also knew how abundant the different species were from previous field studies. I’ll take the hypotheses one by one to show what we found: Eye of the beholder hypothesis – We compared human rankings and the similarity based on measurements and found that there was a strong correlation. We already knew that human rankings correlate with bird rankings of fidelity (from a previous study) so this suggests that it isn’t human vision that is giving the appearance of poor mimics – those mimics really are poor. Multi-model hypothesis – Comparing measurements of species, we saw that all of the hover flies closely resembled one another, all of the wasps closely resembled one another and all of the bees closely resembled one another. There was no evidence that any of the hover flies are intermediate between two models. Kin selection hypothesis – First of all, the kin selection hypothesis requires that closely related individuals remain close together (so offspring don’t move far from their parents, and siblings from their siblings). However, hover flies fly considerable distances making this unlikely. Second, we would expect that the mimetic fidelity of a species would decrease as abundance increased. This prediction arises because a larger number of hover flies would make it more likely that avian predators would try to eat them. There is, therefore, a greater pressure on maintaining mimetic imperfection so that the benefits of some similarity are retained. We found that there is no evidence of a negative relationship between abundance (measured in field studies) and mimetic fidelity. Constraints hypothesis – Due to the diversity of potential explanations for constraints, this is really a series of hypotheses and we couldn’t demonstrate that constraints were not playing a role somehow. However… Relaxed selection hypothesis – When we looked at the relationship between body size and mimetic fidelity there was a very strong relationship. Species that had larger bodies were much better mimics than species that were smaller. This is easily explained by looking at which species of hover fly would be most profitable for a bird to attack. If you are a big, juicy hover fly, birds are going to attack you more because it is worth chasing you. If you are a small hover fly then birds will not bother. As a result, selection is relaxed on smaller species and so those species do not evolve a high degree of mimetic fidelity. Conclusion We demonstrated that variation in mimetic fidelity in hover flies is very likely due to lower predation on smaller, less profitable species leading to relaxed selection for mimetic perfection. There are a few alternative hypotheses tied up in the “constraints” hypothesis that we cannot discount, but the strength of this relationship suggests that they are relatively minor. Of course, the next step is to test this theory in other systems, including the evolution of eye spots in caterpillars. We already have some anecdotal evidence that larger caterpillars tend to be better mimics, but we are busy testing that right now so watch this space!

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