Dr Emmanuelle Briolat

© 2019 Caro et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Averting attack by biting flies is increasingly regarded as the evolutionary driver of zebra stripes, although the precise mechanism by which stripes ameliorate attack by ectoparasites is unknown. We examined the behaviour of tabanids (horse flies) in the vicinity of captive plains zebras and uniformly coloured domestic horses living on a horse farm in Britain. Observations showed that fewer tabanids landed on zebras than on horses per unit time, although rates of tabanid circling around or briefly touching zebra and horse pelage did not differ. In an experiment in which horses sequentially wore cloth coats of different colours, those wearing a striped pattern suffered far lower rates of tabanid touching and landing on coats than the same horses wearing black or white, yet there were no differences in attack rates to their naked heads. In separate, detailed video analyses, tabanids approached zebras faster and failed to decelerate before contacting zebras, and proportionately more tabanids simply touched rather than landed on zebra pelage in comparison to horses. Taken together, these findings indicate that, up close, striped surfaces prevented flies from making a controlled landing but did not influence tabanid behaviour at a distance. To counteract flies, zebras swished their tails and ran away from fly nuisance whereas horses showed higher rates of skin twitching. As a consequence of zebras’ striping, very few tabanids successfully landed on zebras and, as a result of zebras’ changeable behaviour, few stayed a long time, or probed for blood.

Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency‐dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator–prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once‐paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.