Automimicry destabilizes aposematism: predator sample-and-reject behaviour may provide a solution

Aposematic (warning) signals of prey help predators to recognize the defended distasteful or poisonous prey that should be avoided. The evolution of aposematism in the context of predation has been in the center of modern ecology for a long time. But, the possible roles of aposematic signals in other ecological contexts have been largely ignored. Here we address the role of aposematic signals in competition between prey and predators. Bumblebees use visual and auditory aposematic signals to warn predators about their defenses. For 2 years, we observed competition for nestboxes between chemically defended insects, Bombus ardens (and possibly also Bombus ignitus), and cavity nesting birds (Parus minor and Poecile varius). Bumblebees settled in 16 and 9 % of nestboxes (in 2010 and 2011 breeding seasons, respectively) that contained bird nests at the advanced stage of nest building or at the stage of egg laying. Presence of bumblebees prevented the birds from continuing the breeding activities in the nestboxes, while insects took over the birds’ nests (a form of kleptoparasitism). Playback experiments showed that the warning buzz by bumblebees contributed to the success in ousting the birds from their nests. This demonstrates that aposematic signals may be beneficial also in the context of resource competition.Electronic supplementary materialThe online version of this article (doi:10.1007/s00265-013-1553-2) contains supplementary material, which is available to authorized users.

BackgroundIn contrast to traditional models of purifying selection and a single aposematic signal in Müllerian complexes, some communities of unprofitable prey contain members with multiple aposematic patterns. Processes responsible for diversity in aposematic signaling are poorly understood and large multi-species communities are seldom considered.ResultsWe analyzed the phylogeny and aposematic patterns of closely related Eniclases net-winged beetles in New Guinea using mtDNA and nextRAD data. We suggest three clades of closely related and incompletely reproductively isolated lineages, detail the extent of polymorphism among Eniclases, and categorize their low-contrast aposematic patterns. The warning signal of Eniclases consists of body shape and color, with ambiguous color perception under some circumstances, i.e., when resting on the undersides of leaves. Field observations suggest that perception of the aposematic signal is affected by beetle behavior and environmental conditions. Local communities containing Eniclases consisted of 7–85 metriorrhynchine species assigned to 3–10 colour patterns.ConclusionAs a result, we suggest that under certain light conditions the aposematic colour signal is less apparent than the body shape in net-winged beetle communities. We document variable environmental factors in our study area and highly diverse multi-species communities of other net-winged beetles. Which implies dynamically changing community structure in space and time. Variable environmental conditions and diverse community composition are suggested to be favorable for the persistence of multiple aposematic patterns, imperfect mimics, and intraspecific polymorphism. Further research should identify the relative effect of these factors on purifying selection and the alleles which are responsible for phenotypic differences.

The diversity of aposematic signals is one of the most difficult phenomena for understanding the evolution of such signals because aposematic animals are most effectively protected when they are common. Theoretical and experimental studies predict that a combination of local selection pressures could maintain variation in aposematic signals. However, the application of this hypothesis to large-scale geographic variation in aposematic signals, other than mimicry systems, is yet to be tested empirically. I investigated geographic variation in morphological and behavioural aposematic signals of the newts, Cynops pyrrhogaster, and in predation pressures on them in populations ranging over 800 km of latitude. Field experiments demonstrated that local differences in predation pressures explain well the island-mainland variation in the aposematic colouration and behaviour of newts. Furthermore, I found a latitudinal gradient in aposematic colouration but not in behaviour, independent of predation pressures. The results suggested that island-mainland variation in aposematic signals resulting from local differences in predation pressures might also be shaped by several factors, such as temperature, body size variation, and genetic differences, and such factors might act on each aposematic trait differently.

Despite accumulating evidence for selection within natural systems, the importance of random genetic drift opposing Wright's and Fisher's views of evolution continue to be a subject of controversy. The geographical diversification of aposematic signals appears to be a suitable system to assess the factors involved in the process of adaptation since both theories were independently proposed to explain this phenomenon. In the present study, the effects of drift and selection were assessed from population genetics and predation experiments on poison-dart frogs, Ranitomaya imitator, of Northern Peru. We specifically focus on the transient zone between two distinct aposematic signals. In contrast to regions where high predation maintains a monomorphic aposematic signal, the transient zones are characterized by lowered selection and a high phenotypic diversity. As a result, the diversification of phenotypes may occur via genetic drift without a significant loss of fitness. These new phenotypes may then colonize alternative habitats if successfully recognized and avoided by predators. This study highlights the interplay between drift and selection as determinant processes in the adaptive diversification of aposematic signals. Results are consistent with the expectations of the Wright's shifting balance theory and represent, to our knowledge, the first empirical demonstration of this highly contested theory in a natural system.

An apparent and common feature of aposematic patterns is that they contain a high level of achromatic (luminance) contrast, for example, many warning signals combine black spots and stripes with a lighter colour such as yellow. However, the potential importance of achromatic contrast, as distinct from colour contrast, in reducing predation has been largely overlooked. Here, using domestic chicks as a model predator, we manipulated the degree of achromatic contrast in warning patterns to test if high luminance contrast in aposematic signals is important for deterring naïve predators. We found that the chicks were less likely to approach and eat prey with high contrast compared to low contrast patterns. These findings suggest that aposematic prey patterns with a high luminance contrast can benefit from increased survival through eliciting unlearned biases in naïve avian predators. Our work also highlights the importance of considering luminance contrast in future work investigating why aposematic patterns take the particular forms that they do.

Investigating the subjective reports of rejection processes in the word frequency mirror effect

Recognizing form and function of animal defenses is paramount to understanding the ecological and evolutionary forces behind predator and prey dynamics. Color patterns are strongly related to defensive strategies in animals. Some rely on camouflage to avoid detection, while others are brightly colored and conspicuously signal their noxiousness to potential predators. Still others combine cryptic dorsal coloration with colorful patches that are concealed in resting position but are facultatively unveiled by special behavior or simply during activity. Such hidden conspicuous color patches may be an intermediate stage in the evolution from camouflage to aposematism. Many species, especially treefrogs of the family Hylidae, are generally considered to be cryptic, yet show colorful patches on their flanks or thighs and have defensive skin secretions that may have unpalatable properties. We investigated whether the conspicuous black and yellow spotted pattern on the thighs of Eastern Gray Treefrogs (Hyla versicolor) serve as an aposematic signal. We conducted a palatability study to test whether Gray Treefrog skin secretions are unpalatable, and a clay model field study to test whether the conspicuous black and yellow thigh pattern is an aposematic warning coloration that reduces predation. Frog secretions were discriminated against during palatability assays, and clay models painted with a spotted black and yellow pattern suffered lower predation rates. Our findings support the hypothesis that hidden color patches act as aposematic signals in Gray Treefrogs and suggest that more species benefit from aposematic coloration than currently appreciated.

Aposematic species use brightly coloured signals to warn potential predators of their unpalatability. The function of these signals is largely believed to be frequency-dependent. All else being equal, stabilizing selection is expected to constrain the evolution of novel signals. However, despite the expected frequency-dependent function of aposematic signals, interpopulation variation in aposematic signals is ubiquitous in nature. Here, we used clay models of the poison frog Dendrobates tinctorius to test the nature of selection in regions containing varying frequencies of frogs possessing the local aposematic signal. Our findings support a role for stabilizing selection in maintaining the local signal type in a region of high signal frequency; however, we observe a lack of stabilizing selection at one site coincident with a decrease in the density of frogs possessing the local signal. Spatial variation in local aposematic signal frequencies may facilitate the evolution of novel signal types by altering the adaptive landscape for divergent aposematic phenotypes. Our results provide evidence for spatial variation in the selective regime acting on aposematic signals within an established aposematic system and highlight the need for further study of the nature of selection acting across different spatial scales in diverse aposematic systems.

It is commonly assumed that natural selection imposed by predators is the prevailing force driving the evolution of aposematic traits. Here, we demonstrate that aposematic signals are shaped by sexual selection as well. We evaluated sexual selection for coloration brightness in populations of the poison frog Oophaga [Dendrobates] pumilio in Panama's Bocas del Toro archipelago. We assessed female preferences for brighter males by manipulating the perceived brightness of spectrally matched males in two-way choice experiments. We found strong female preferences for bright males in two island populations and weaker or ambiguous preferences in females from mainland populations. Spectral reflectance measurements, coupled with an O. pumilio-specific visual processing model, showed that O. pumilio coloration was significantly brighter in island than in mainland morphs. In one of the island populations (Isla Solarte), males were significantly more brightly colored than females. Taken together, these results provide evidence for directional sexual selection on aposematic coloration and document sexual dimorphism in vertebrate warning coloration. Although aposematic signals have long been upheld as exemplars of natural selection, our results show that sexual selection should not be ignored in studies of aposematic evolution.

Colour alone matters: no predator generalization among morphs of an aposematic moth

Conspicuous coloration coupled with secondary defensive mechanisms is known as aposematic coloration and is used in predator avoidance and defense. Classic theory argues that aposematic signals tend to be more effective in larger organisms as they are intrinsically more easily detected by predators and are also more profitable prey items. Thus, it has been hypothesized that conspicuous coloration evolves in tandem with increased body size in aposematic prey because this likely increases the visibility and efficacy of the signal. To test this hypothesis, we used a comparative phylogenetic approach to investigate associations between body size and conspicuous coloration in two North American salamander genera: Ambystoma and Plethodon, both of which secrete noxious compounds to deter predators. Our analyses showed that increased conspicuous coloration co-evolved with increased body size in Ambystoma, yet we found the opposite relationship in the Plethodon clade. We speculate this is likely because Ambystoma are generally larger than Plethodon and exhibit gregarious mating behavior. Future studies should explore the toxicity of slimy skin secretions and how this may contribute to aposematic signaling in salamanders.

Consumer clusters in Denmark based on coarse vegetable intake frequency, explained by hedonics, socio-demographic, health and food lifestyle factors. A cross-sectional national survey

Many organisms use warning, or aposematic, coloration to signal their unprofitability to potential predators. Aposematically colored prey are highly visually conspicuous. There is considerable empirical support that conspicuousness promotes the effectiveness of the aposematic signal. From these experiments, it is well documented that conspicuous, unprofitable prey are detected sooner and aversion learned faster by the predator as compared with cryptic, unprofitable prey. Predators also retain memory of the aversion longer when prey is conspicuous. The present study focused on the elements of conspicuousness that confer these benefits of aposematic coloration. Drawing on current understanding of animal vision, we distinguish 2 features of warning coloration: high chromatic contrast and high brightness, or luminance, contrast. Previous investigations on aposematic signal efficacy have focused mainly on the role of high chromatic contrast between prey and background, whereas little research has investigated the role of high luminance contrast. Using the Chinese mantid as a model predator and gray-painted milkweed bugs as model prey, we found that increased prey luminance contrast increased detection of prey, facilitated predator aversion learning, and increased predator memory retention of the aversive response. Our results suggest that the luminance contrast component of aposematic coloration can be an effective warning signal between the prey and predator. Thus, warning coloration can even evolve as an effective signal to color blind predators. Copyright 2007.

The effects of electrical vestibular stimulation upon movement and perception suggest two evoked sensations: head roll and inter-aural linear acceleration. The head roll vector causes walking subjects to turn in a direction dependent on head pitch, requiring generation of torque around a vertical axis. Here the effect of vestibular stimulation upon vertical torque (T(z)) was investigated during quiet stance. With the head tilted forward, square-wave stimuli applied to the mastoid processes evoked a polarity-specific T(z) response accompanied by trunk yaw. Stochastic vestibular stimulation (SVS) was used to investigate the effect of head pitch with greater precision; the SVS–T(z) cross-correlation displayed a modulation pattern consistent with the head roll vector and this was also reflected by changes in coherence at 2–3 Hz. However, a separate response at 7–8 Hz was unaffected by head pitch. Head translation (rather than rotation) had no effect upon this high frequency response either, suggesting it is not caused by a sense of body rotation induced by an inter-aural acceleration vector offset from the body. Instead, high coherence between medio-lateral shear force and T(z) at the same frequency range suggests it is caused by mechanical coupling to evoked medio-lateral sway. Consistent with this explanation, the 7–8 Hz response was attenuated by 90 deg head roll or yaw, both of which uncouple the inter-aural axis from the medio-lateral sway axis. These results demonstrate two vertical torque responses to electrical vestibular stimulation in standing subjects. The high frequency response can be attributed to mechanical coupling to evoked medio-lateral sway. The low frequency response is consistent with a reaction to a sensation of head roll, and provides a novel method for investigating proprioceptive-vestibular interactions during stance.

Purpose To compare low- versus high-frequency ultrasonographic (US) elastography for detection of steatohepatitis in rats by using histopathologic findings as the reference standard. Materials and Methods Between March and September 2014, after receiving approval from the institutional animal care committee, 60 male Sprague-Dawley rats were fed either a standard chow for 4 weeks or a methionine- and choline-deficient diet for 1, 4, 8, or 12 weeks to induce a continuum of steatohepatitis severity. Liver shear stiffness was assessed in vivo by using US elastography at low (40-130-Hz) and high (130-220-Hz) frequencies. Histologic features (steatosis, inflammation, and fibrosis) and modified nonalcoholic steatohepatitis categories were used as reference standards. Definite steatohepatitis was divided into steatohepatitis with fibrosis stage 1 or lower and stage 2 and higher. Analyses included the Kendall τ correlation, multivariable linear regression analyses, Kruskal-Wallis rank sum test, and post hoc Dunn test with Holm correction. Results Correlations between liver shear stiffness and histologic features were higher at high frequencies than at low frequencies (low frequency: 0.08, 0.24, and 0.20 for steatosis, inflammation, and fibrosis, respectively; high frequency: 0.11, 0.35, and 0.50, respectively). The absolute value of multivariable regression coefficients was higher at high frequencies for the presence of steatosis, inflammation grade, and fibrosis stage (low frequency: -0.475, 0.157, and 0.209, respectively; high frequency: -0.893, 0.357, and 0.447, respectively). The model fit was better at high frequencies (adjusted R2 = 0.57) than at low frequencies (adjusted R2 = 0.21). There was a significant difference between steatohepatitis categories at both low and high frequencies (P = .022 and P < .001, respectively). Conclusion Liver shear stiffness measured with US elastography provided better distinction of steatohepatitis categories at high frequencies than at low frequencies. Further, liver shear stiffness decreased with steatosis and increased with inflammation and fibrosis at both low and high frequencies. © RSNA, 2016 Online supplemental material is available for this article.