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Camouflage is a widespread and well-studied anti-predator strategy, yet identifying which patterns provide optimal protection in any given scenario remains challenging. Besides the virtually limitless combinations of colours and patterns available to prey, selection for camouflage strategies will depend on complex interactions between prey appearance, background properties and predator traits, across repeated encounters between co-evolving predators and prey. Experiments in artificial evolution, pairing psychophysics detection tasks with genetic algorithms, offer a promising way to tackle this complexity, but sophisticated genetic algorithms have so far been restricted to screen-based experiments. Here, we present methods to test the evolution of colour patterns on physical prey items, under selection from wild predators in the field. Our techniques expand on a recently-developed open-access pattern generation and genetic algorithm framework, modified to operate alongside artificial predation experiments. In this system, predators freely interact with prey, and the order of attack determines the survival and reproduction of prey patterns into future generations. We demonstrate the feasibility of these methods with a case study, in which free-flying birds feed on artificial prey deployed in semi-natural conditions, against backgrounds differing in three-dimensional complexity. Wild predators reliably participated in this experiment, foraging for 11 to 16 generations of artificial prey and encountering a total of 1,296 evolved prey items. Changes in prey pattern across generations indicated improvements in several metrics of similarity to the background, and greater edge disruption, although effect sizes were relatively small. Computer-based replicates of these trials, with human volunteers, highlighted the importance of starting population parameters for subsequent evolution, a key consideration when applying these methods. Ultimately, these methods provide pathways for integrating complex genetic algorithms into more naturalistic predation trials. Customisable open-access tools should facilitate application of these tools to investigate a wide range of visual pattern types in more ecologically-relevant contexts., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Briolat 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.)

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies., (© 2023 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

Background-matching camouflage is a well-established strategy to reduce detection, but implementing this on heterogeneous backgrounds is challenging. For prey with fixed color patterns, solutions include specializing on a particular visual microhabitat, or adopting a compromise or generalist appearance, matching multiple backgrounds less well. Existing studies suggest both approaches can succeed, but most consider relatively simple scenarios, where artificial prey appear against two backgrounds differing in a single visual characteristic. Here, we used computer-based search tasks with human participants to test the relative benefits of specializing and generalizing for complex targets, displayed on either two or four types of naturalistic backgrounds. Across two background types, specialization was beneficial on average. However, the success of this strategy varied with search duration, such that generalist targets could outperform specialists over short search durations due to the presence of poorly matched specialists. Over longer searches, the remaining well-matched specialists had greater success than generalists, leading to an overall benefit of specialization at longer search durations. Against four different backgrounds, the initial cost to specialization was greater, so specialists and generalists ultimately experienced similar survival. Generalists performed better when their patterning was a compromise between backgrounds that were more similar to each other than when backgrounds were more different, with similarity in luminance more relevant than pattern differences. Time dependence in the relative success of these strategies suggests that predator search behavior may affect optimal camouflage in real-world situations., Competing Interests: We declare we have no conflicts of interest., (© The Author(s) 2023. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology.)

Background: Crypsis by background-matching is a critical form of anti-predator defence for animals exposed to visual predators, but achieving effective camouflage in patchy and variable natural environments is not straightforward. To cope with heterogeneous backgrounds, animals could either specialise on particular microhabitat patches, appearing cryptic in some areas but mismatching others, or adopt a compromise strategy, providing partial matching across different patch types. Existing studies have tested the effectiveness of compromise strategies in only a limited set of circumstances, primarily with small targets varying in pattern, and usually in screen-based tasks. Here, we measured the detection risk associated with different background-matching strategies for relatively large targets, with human observers searching for them in natural scenes, and focusing on colour. Model prey were designed to either 'specialise' on the colour of common microhabitat patches, or 'generalise' by matching the average colour of the whole visual scenes., Results: In both the field and an equivalent online computer-based search task, targets adopting the generalist strategy were more successful in evading detection than those matching microhabitat patches. This advantage occurred because, across all possible locations in these experiments, targets were typically viewed against a patchwork of different microhabitat areas; the putatively generalist targets were thus more similar on average to their various immediate surroundings than were the specialists., Conclusions: Demonstrating close agreement between the results of field and online search experiments provides useful validation of online citizen science methods commonly used to test principles of camouflage, at least for human observers. In finding a survival benefit to matching the average colour of the visual scenes in our chosen environment, our results highlight the importance of relative scales in determining optimal camouflage strategies, and suggest how compromise coloration can succeed in nature., (© 2021. The Author(s).)

The nighttime environment is being altered rapidly over large areas worldwide through introduction of artificial lighting, from streetlights and other sources. This is predicted to impact the visual ecology of many organisms, affecting both their intra- and interspecific interactions. Here, we show the effects of different artificial light sources on multiple aspects of hawkmoth visual ecology, including their perception of floral signals for pollination, the potential for intraspecific sexual signalling, and the effectiveness of their visual defences against avian predators. Light sources fall into three broad categories: some that prevent use of chromatic signals for these behaviours, others that more closely mimic natural lighting conditions, and, finally, types whose effects vary with light intensity and signal colour. We find that Phosphor Converted (PC) amber LED lighting - often suggested to be less harmful to nocturnal insects - falls into this third disruptive group, with unpredictable consequences for insect visual ecology depending on distance from the light source and the colour of the objects viewed. The diversity of impacts of artificial lighting on hawkmoth visual ecology alone argues for a nuanced approach to outdoor lighting in environmentally sensitive areas, employing intensities and spectra designed to limit those effects of most significant concern.

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., (© 2018 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.)

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., Competing Interests: The authors have declared that no competing interests exist.

Many defended species use conspicuous visual warning signals to deter potential predators from attacking. Traditional theory holds that these signals should converge on similar forms, yet variation in visual traits and the levels of defensive chemicals is common, both within and between species. It is currently unclear how the strength of signals and potency of defences might be related: conflicting theories suggest that aposematic signals should be quantitatively honest, or, in contrast, that investment in one component should be prioritized over the other, while empirical tests have yielded contrasting results. Here, we advance this debate by examining the relationship between defensive chemicals and signal properties in a family of aposematic Lepidoptera, accounting for phylogenetic relationships and quantifying coloration from the perspective of relevant predators. We test for correlations between toxin levels and measures of wing colour across 14 species of day-flying burnet and forester moths (Lepidoptera: Zygaenidae), protected by highly aversive cyanogenic glucosides, and find no clear evidence of quantitative signal honesty. Significant relationships between toxin levels and coloration vary between sexes and sampling years, and several trends run contrary to expectations for signal honesty. Although toxin concentration is positively correlated with increasing luminance contrast in forewing pattern in 1 year, higher toxin levels are also associated with paler and less chromatically salient markings, at least in females, in another year. Our study also serves to highlight important factors, including sex-specific trends and seasonal variation, that should be accounted for in future work on signal honesty in aposematic species., (© 2018 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

The distinctive black and red wing pattern of six-spot burnet moths (Zygaena filipendulae, L.) is a classic example of aposematism, advertising their potent cyanide-based defences. While such warning signals provide a qualitatively honest signal of unprofitability, the evidence for quantitative honesty, whereby variation in visual traits could provide accurate estimates of individual toxicity, is more equivocal. Combining measures of cyanogenic glucoside content and wing color from the perspective of avian predators, we investigate the relationship between coloration and defences in Z. filipendulae, to test signal honesty both within and across populations. There were no significant relationships between mean cyanogenic glucoside concentration and metrics of wing coloration across populations in males, yet in females higher cyanogenic glucoside levels were associated with smaller and lighter red forewing markings. Trends within populations were similarly inconsistent with quantitative honesty, and persistent differences between the sexes were apparent: larger females, carrying a greater total cyanogenic glucoside load, displayed larger but less conspicuous markings than smaller males, according to several color metrics. The overall high aversiveness of cyanogenic glucosides and fluctuations in color and toxin levels during an individual's lifetime may contribute to these results, highlighting generally important reasons why signal honesty should not always be expected in aposematic species., (© 2018 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.)