Does spatial variation in predation pressure modulate selection for aposematism?
ABSTRACT: It is widely believed that aposematic signals should be conspicuous, but in nature, they vary from highly conspicuous to near cryptic. Current theory, including the honest signal or trade-off hypotheses of the toxicity-conspicuousness relationship, cannot explain why adequately toxic species vary substantially in their conspicuousness. Through a study of similarly toxic Danainae (Nymphalidae) butterflies and their mimics that vary remarkably in their conspicuousness, we show that the benefits of conspicuousness vary along a gradient of predation pressure. Highly conspicuous butterflies experienced lower avian attack rates when background predation pressure was low, but attack rates increased rapidly as background predation pressure increased. Conversely, the least conspicuous butterflies experienced higher attack rates at low predation pressures, but at high predation pressures, they appeared to benefit from crypsis. Attack rates of intermediately conspicuous butterflies remained moderate and constant along the predation pressure gradient. Mimics had a similar pattern but higher attack rates than their models and mimics tended to imitate the signal of less attacked model species along the predation pressure gradient. Predation pressure modulated signal fitness provides a possible mechanism for the maintenance of variation in conspicuousness of aposematic signals, as well as the initial survival of conspicuous signals in cryptic populations in the process of aposematic signal evolution, and an alternative explanation for the evolutionary gain and loss of mimicry.
Project description:Natural selection is widely noted to drive divergence of phenotypic traits. Predation pressure can facilitate morphological divergence, for example the evolution of both cryptic and conspicuous coloration in animals. In this context Dendrobatid frogs have been used to study evolutionary forces inducing diversity in protective coloration. The polytypic strawberry poison frog (Oophaga pumilio) shows strong divergence in aposematic coloration among populations. To investigate whether predation pressure is important for color divergence among populations of O. pumilio we selected four mainland populations and two island populations from Costa Rica and Panama. Spectrometric measurements of body coloration were used to calculate color and brightness contrasts of frogs as an indicator of conspicuousness for the visual systems of several potential predators (avian, crab and snake) and a conspecific observer. Additionally, we conducted experiments using clay model frogs of different coloration to investigate whether the local coloration of frogs is better protected than non-local color morphs, and if predator communities vary among populations. Overall predation risk differed strongly among populations and interestingly was higher on the two island populations. Imprints on clay models indicated that birds are the main predators while attacks of other predators were rare. Furthermore, clay models of local coloration were equally likely to be attacked as those of non-local coloration. Overall conspicuousness (and brightness contrast) of local frogs was positively correlated with attack rates by birds across populations. Together with results from earlier studies we conclude that conspicuousness honestly indicates toxicity to avian predators. The different coloration patterns among populations of strawberry poison frogs in combination with behavior and toxicity might integrate into equally efficient anti-predator strategies depending on local predation and other ecological factors.
Project description:Many organisms have evolved adaptive coloration that reduces their risk of predation. Cryptic coloration reduces the likelihood of detection/recognition by potential predators, while warning or aposematic coloration advertises unprofitability and thereby reduces the likelihood of attack. Although some studies show that aposematic coloration functions better at decreasing attack rate than crypsis, recent work has suggested and demonstrated that crypsis and aposematism are both successful strategies for avoiding predation. Furthermore, the visual environment (e.g., ambient lighting, background) affects the ability for predators to detect prey. We investigated these 2 related hypotheses using 2 well-known visually aposematic species of <i>Heliconius</i> butterflies, which occupy different habitats (open-canopy vs. closed-canopy), and one palatable, cryptic, generalist species <i>Junonia coenia</i>. We tested if the differently colored butterflies differ in attack rates by placing plasticine models of each of the 3 species in 2 different tropical habitats where the butterflies naturally occur: disturbed, open-canopy habitat and forested, closed-canopy habitat. The cryptic model had fewer attacks than one of the aposematic models. Predation rates differed between the 2 habitats, with the open habitat having much higher predation. However, we did not find an interaction between species and habitat type, which is perplexing due to the different aposematic phenotypes naturally occurring in different habitats. Our findings suggest that during the Panamanian dry season avian predation on perched butterflies is not a leading cause in habitat segregation between the 2 aposematic species and demonstrate that cryptically colored animals at rest may be better than aposematic prey at avoiding avian attacks in certain environments.
Project description:Behavioral ecologists and evolutionary biologists have long studied how predators respond to prey items novel in color and pattern. Because a predatory response is influenced by both the predator's ability to detect the prey and a post-detection behavioral response, variation among prey types in conspicuousness may confound inference about post-prey-detection predator behavior. That is, a relatively high attack rate on a given prey type may result primarily from enhanced conspicuousness and not predators' direct preference for that prey. Few studies, however, account for such variation in conspicuousness. In a field experiment, we measured predation rates on clay replicas of two aposematic forms of the poison dart frog Dendrobates pumilio, one novel and one familiar, and two cryptic controls. To ask whether predators prefer or avoid a novel aposematic prey form independently of conspicuousness differences among replicas, we first modeled the visual system of a typical avian predator. Then, we used this model to estimate replica contrast against a leaf litter background to test whether variation in contrast alone could explain variation in predator attack rate. We found that absolute predation rates did not differ among color forms. Predation rates relative to conspicuousness did, however, deviate significantly from expectation, suggesting that predators do make post-detection decisions to avoid or attack a given prey type. The direction of this deviation from expectation, though, depended on assumptions we made about how avian predators discriminate objects from the visual background. Our results show that it is important to account for prey conspicuousness when investigating predator behavior and also that existing models of predator visual systems need to be refined.
Project description:Aposematic signals are often characterized by high conspicuousness. Larger and brighter signals reinforce avoidance learning, distinguish defended from palatable prey and are more easily memorized by predators. Conspicuous signalling, however, has costs: encounter rates with naive, specialized or nutritionally stressed predators are likely to increase. It has been suggested that intermediate levels of aposematic conspicuousness can evolve to balance deterrence and detectability, especially for moderately defended species. The effectiveness of such signals, however, has not yet been experimentally tested under field conditions. We used dough caterpillar-like baits to test whether reduced levels of aposematic conspicuousness can have survival benefits when predated by wild birds in natural conditions. Our results suggest that, when controlling for the number and intensity of internal contrast boundaries (stripes), a reduced-conspicuousness aposematic pattern can have a survival advantage over more conspicuous signals, as well as cryptic colours. Furthermore, we find a survival benefit from the addition of internal contrast for both high and low levels of conspicuousness. This adds ecological validity to evolutionary models of aposematic saliency and the evolution of honest signalling.
Project description:Population divergence in sexual signals may lead to speciation through prezygotic isolation. Sexual signals can change solely due to variation in the level of natural selection acting against conspicuousness. However, directional mate choice (i.e., favoring conspicuousness) across different environments may lead to gene flow between populations, thereby delaying or even preventing the evolution of reproductive barriers and speciation. In this study, we test whether natural selection through predation upon mate-choosing females can favor corresponding changes in mate preferences. Our study system, <i>Oophaga pumilio</i>, is an extremely color polymorphic neotropical frog with two distinctive antipredator strategies: aposematism and crypsis. The conspicuous coloration and calling behavior of aposematic males may attract both cryptic and aposematic females, but predation may select against cryptic females choosing aposematic males. We used an experimental approach where domestic fowl were encouraged to find digitized images of cryptic frogs at different distances from aposematic partners. We found that the estimated survival time of a cryptic frog was reduced when associating with an aposematic partner. Hence, predation may act as a direct selective force on female choice, favoring evolution of color assortative mating that, in turn, may strengthen the divergence in coloration that natural selection has generated.
Project description:The direction and strength of selection for prey colouration by predators vary in space and time and depend on the composition of the predator community. We tested the hypothesis that bird selection pressure on prey colouration changes through the season due to changes in the proportion of naïve juvenile individuals in the bird community, because naïve and educated birds differ in their responses to prey colours. Bird predation on caterpillar-shaped plasticine models in two boreal forest sites increased sevenfold from early summer to mid-summer, and the time of this increase coincides with the fledging of juvenile birds. In early summer, cryptic (black and green) models were attacked at fivefold higher rates compared with conspicuous (red and yellow) models. By contrast, starting from fledging time, cryptic and conspicuous models were attacked at similar rates, hinting at a lower selectivity by naïve juvenile birds compared with educated adult birds. Cryptic models exposed in a group together with conspicuous models were attacked by birds at a threefold lower rate than cryptic models exposed singly, thus supporting the aposematic commensalism hypothesis. However, this effect was not observed in mid- and late summer, presumably due to the lack of avoidance of conspicuous prey by the juvenile birds. We conclude that selection pressure on prey colouration weakens considerably when naïve birds dominate in the community, because the survival advantages of aposematic colouration are temporarily lost for both the conspicuous and their neighbouring cryptic prey.
Project description:Many animals advertise their chemical defense to predators with conspicuous coloration and unpalatability, but little is known about the information in these signal elements. To effectively avoid predation, is it more advantageous to invest in increased conspicuousness or greater noxiousness, or to allocate equally to both signal modalities? Using natural variation among poison frog species measured with spectral reflectance and toxicity assays, we tested the relative importance of warning signal components with predator-learning and avoidance experiments. We demonstrate that closely related species use alternative strategies: increasing either conspicuousness or toxicity affords equivalent avoidance by predators and provides protection to nontoxic mimic species. These equally effective predator avoidance tactics demonstrate different aposematic solutions for two potentially costly signal components, providing a mechanism for natural diversity in warning signals.
Project description: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.
Project description:Batesian mimics gain protection from predation through the evolution of physical similarities to a model species that possesses anti-predator defences. This protection should not be effective in the absence of the model since the predator does not identify the mimic as potentially dangerous and both the model and the mimic are highly conspicuous. Thus, Batesian mimics should probably encounter strong predation pressure outside the geographical range of the model species. There are several documented examples of Batesian mimics occurring in locations without their models, but the evolutionary responses remain largely unidentified. A mimetic species has four alternative evolutionary responses to the loss of model presence. If predation is weak, it could maintain its mimetic signal. If predation is intense, it is widely presumed the mimic will go extinct. However, the mimic could also evolve a new colour pattern to mimic another model species or it could revert back to its ancestral, less conspicuous phenotype. We used molecular phylogenetic approaches to reconstruct and test the evolution of mimicry in the North American admiral butterflies (Limenitis: Nymphalidae). We confirmed that the more cryptic white-banded form is the ancestral phenotype of North American admiral butterflies. However, one species, Limenitis arthemis, evolved the black pipevine swallowtail mimetic form but later reverted to the white-banded more cryptic ancestral form. This character reversion is strongly correlated with the geographical absence of the model species and its host plant, but not the host plant distribution of L. arthemis. Our results support the prediction that a Batesian mimic does not persist in locations without its model, but it does not go extinct either. The mimic can revert back to its ancestral, less conspicuous form and persist.
Project description:Complex phenotypes can be modeled as networks of component traits connected by genetic, developmental, or functional interactions. Aposematism, which has evolved multiple times in poison frogs (Dendrobatidae), links a warning signal to a chemical defense against predators. Other traits are involved in this complex phenotype. Most aposematic poison frogs are ant specialists, from which they sequester defensive alkaloids. We found that aposematic species have greater aerobic capacity, also related to diet specialization. To characterize the aposematic trait network more fully, we analyzed phylogenetic correlations among its hypothesized components: conspicuousness, chemical defense, diet specialization, body mass, active and resting metabolic rates, and aerobic scope. Conspicuous coloration was correlated with all components except resting metabolism. Structural equation modeling on the basis of trait correlations recovered "aposematism" as one of two latent variables in an integrated phenotypic network, the other being scaling with body mass and physiology ("scale"). Chemical defense and diet specialization were uniquely tied to aposematism whereas conspicuousness was related to scale. The phylogenetic distribution of the aposematic syndrome suggests two scenarios for its evolution: (i) chemical defense and conspicuousness preceded greater aerobic capacity, which supports the increased resource-gathering abilities required of ant-mite diet specialization; and (ii) assuming that prey are patchy, diet specialization and greater aerobic capacity evolved in tandem, and both traits subsequently facilitated the evolution of aposematism.