Sole coloration as an unusual aposematic signal in a Neotropical toad

Many animals have evolved remarkable strategies to avoid predation. In diurnal, toxic harlequin toads (Atelopus) from the Amazon basin, we find a unique colour signal. Some Atelopus populations have striking red soles of the hands and feet, visible only when walking. When stationary, the toads are hard to detect despite their yellow-black dorsal coloration. Consequently, they switch between high and low conspicuousness. Interestingly, some populations lack the extra colour display of the soles. We found comprehensive support that the red coloration can act as an aposematic signal directed towards potential predators: red soles are significantly more conspicuous than soles lacking red coloration to avian predators and the presence of the red signal significantly increases detection. Further, toads with red soles show bolder behaviour by using higher sites in the vegetation than those lacking this signal. Field experiments hint at a lower attack risk for clay models with red soles than for those lacking the signal, in a population where the red soles naturally occur. We suggest that the absence of the signal may be explained by a higher overall attack risk or potential differences of predator community structure between populations. © 2019, The Author(s)

Forewing marking coloration and cyanogenic glucoside data for Zygaenidae in this study

This file contains all the data for the main analyses in this study: specimen info (ID, species, collection year and locality, sex, mass), coloration metrics (% forewing area, luminance, saturation, hue, internal contrasts with wing ground colour), and cyanogenic glucoside data (total amounts and concentration of linamarin, lotaustralin and total cyanogenic glucosides). Note: Hue 1 corresponds to the hue channel used in the paper; Hue 2 is based on the second principal component generated by PCA, and was not used in the final analyses. FW=Forewing

Cyanogenic glucoside levels - original data and 2017 re-run

This file presents data for the 20 specimens for which LC-MS quantification of cyanogenic glucosides was re-run in 2017. It contains specimen information and cyanogenic glucoside data for the original run (data analysed in 2015 and 2016, when the samples were collected) and for the new run in 2017, when samples from 2015 and 2016 were analysed together

Adapting genetic algorithms for artificial evolution of visual patterns under selection from wild predators.

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

Data from: No evidence of quantitative signal honesty across species of aposematic burnet moths (Lepidoptera: Zygaenidae)

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 prioritised 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 one 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

Diversity in warning coloration: selective paradox or the norm?

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

The evolution and ecology of multiple antipredator defences

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.publishe

The evolution and ecology of multiple antipredator defences

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.ISSN:1010-061XISSN:1420-910

The evolution and ecology of multiple antipredator defences

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