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... At the Nouragues Natural Reserve, French Guiana, the frogs are blue-black with a bright yellow ring, which may be broken or joined to form a figure eight ( Fig. 1A) (34). However, the presence of asymmetry and variation between individuals does not conform to standard aposematic theory (34,35), and is reminiscent of cryptic patterning Significance Poison dart frogs are well known for their deadly toxins and bright colors; they are a classic example of warning coloration. However, conspicuousness is not the only consideration; defensive coloration must be effective against a diverse predator community with a variety of different visual systems, and variable knowledge of prey defenses and motivation to attack. ...
... It has further been suggested that the colors of D. tinctorius may disrupt a predator's ability to track a moving frog (motion dazzle) (48,49) and that phenotypic variation may trade off the benefits of salient signaling versus camouflage (35). We propose pattern-blending as an additional (albeit not mutually exclusive) Fig. 3. Time taken by human observers to detect frogs at the near and far distances. ...
... More research is needed to understand how multiple functions interact under different viewing conditions [e.g., lighting conditions (35)/viewing distance and angle], in different contexts [e.g., microhabitats (35)/posture and motion (48,49)], and to different observers (predators and conspecifics), as well as how color is affected by temporal changes in behavior, toxicity, and the visual environment. Furthermore, intraspecific variation both within (seemingly continuous) (35,48) and between (largely discrete) (42,43,54,55) populations suggests this balance in selection pressures may vary both geographically and between individuals. However, it is currently unknown whether these differences are the result of natural or sexual selection, or neutral drift within a broad definition of the aposematic signal defined by potential predators. ...
Article
Poison dart frogs provide classic examples of warning signals: potent toxins signaled by distinctive, conspicuous coloration. We show that, counterintuitively, the bright yellow and blue-black color of Dendrobates tinctorius (Dendrobatidae) also provides camouflage. Through computational modeling of predator vision, and a screen-based detection experiment presenting frogs at different spatial resolutions, we demonstrate that at close range the frog is highly detectable, but from a distance the colors blend together, forming effective camouflage. This result was corroborated with an in situ experiment, which found survival to be background-dependent, a feature more associated with camouflage than aposematism. Our results suggest that in D. tinctorius the distribution of pattern elements, and the particular colors expressed, act as a highly salient close range aposematic signal, while simultaneously minimizing detectability to distant observers.
... In these cases, encounters with receivers are largely unpredictable-that is, they occur under variable visual conditions-and behavioural finetuning of signal delivery is largely unavailable. The signaling niche hypothesis is supported by evidence from sexual and aposematic systems in which selection for effective communication in heterogeneous environments has driven the diversification of visual signals [5,[21][22][23][24][25]. For example, recent experimental work has shown that the polymorphic warning colours of dyeing poison frogs (Dendrobates tinctorius) are differentially detectable to vertebrate predators under varied lighting conditions [25]. ...
... The signaling niche hypothesis is supported by evidence from sexual and aposematic systems in which selection for effective communication in heterogeneous environments has driven the diversification of visual signals [5,[21][22][23][24][25]. For example, recent experimental work has shown that the polymorphic warning colours of dyeing poison frogs (Dendrobates tinctorius) are differentially detectable to vertebrate predators under varied lighting conditions [25]. This variation in ambient light occurs across fine spatial and temporal scales throughout the frogs' natural forest habitat, which may favour the maintenance of signal polymorphism. ...
... Visual signalling systems contain ample sources of variation that may contribute to the maintenance of colour polymorphism. While the role of abiotic variation in establishing 'signalling niches' is well supported [21][22][23][24][25], the question of whether perceptual variation may contribute in a similar manner is largely unexamined. In the first direct test of the possibility, our results implicate the conditional prioritisation of visual information in receivers as a likely contributing factor to the maintenance of colour polymorphism in a deceptive context. ...
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Background Theory predicts that colour polymorphism may be favored by variation in the visual context under which signals are perceived. The context encompasses all environmental determinants of light availability and propagation, but also the dynamics of perception in receivers. Color vision involves the neural separation of information into spectral versus luminance channels, which often differentially guide specific tasks. Here we explicitly tested whether this discrete perceptual basis contributes to the maintenance of polymorphism in a prey-luring system. The orb-weaving spider Gasteracantha fornicata is known to attract a broad community of primarily dipteran prey due to their conspicuous banded dorsal signal. They occur in two morphs (“white” and “yellow”) which should, respectively, generate greater luminance and color contrast in the dipteran eye. Given that arthropods often rely upon luminance-versus-spectral cues for relatively small-versus-large stimulus detection, we predicted a switch in relative attractiveness among morphs according to apparent spider size. ResultsOur experimental tests used colour-naïve individuals of two known prey species (Drosophila hydei and Musca domestica) in replicate Y-maze choice trials designed to manipulate the apparent size of spider models via the distance at which they are viewed. Initial trials confirmed that flies were attracted to each G. fornicata morph in single presentations. When given a simultaneous choice between morphs against a viewing background typical of those encountered in nature, flies exhibited no preference regardless of the visual angle subtended by models. However, when backgrounds were adjusted to nearer the extremes of those of each morph in the wild, flies were more attracted by white morphs when presented at longer range (consistent with a reliance on achromatic cues), yet were unbiased in their close-range choice. Conclusion While not fully consistent with predictions (given the absence of a differential preference for stimuli at close range), our results demonstrate an effect of apparent stimulus size upon relative morph attractiveness in the direction anticipated from present knowledge of fly visual ecology. This implies the potential tuning of G. fornicata morph signal structure according to a perceptual feature that is likely common across their breadth of arthropod prey, and complements recent observational work in suggesting a candidate mechanism for the maintenance of deceptive polymorphism through the exploitation of different visual channels in prey.
... We used data from an experiment in which human viewers were tasked with finding objects under two forest-light environments [12]. The focal stimuli consisted of paraffin wax models of four different morphs of the dyeing poison frog Dendrobates tinctorius (fig. ...
... The focal stimuli consisted of paraffin wax models of four different morphs of the dyeing poison frog Dendrobates tinctorius (fig. 1e-h in [12]), whose patterns differed in the arrangement and constitution of 'yellow', 'blue' and 'black' patches (see [12] for model-construction details). Reflectance spectra (figure 1a) were captured from representative patches using an OceanOptics USB4000-FL spectrometer and a PX-2 pulsed xenon light source, calibrated against a Spectralon (Labsphere, Congleton, UK) white standard. ...
... The focal stimuli consisted of paraffin wax models of four different morphs of the dyeing poison frog Dendrobates tinctorius (fig. 1e-h in [12]), whose patterns differed in the arrangement and constitution of 'yellow', 'blue' and 'black' patches (see [12] for model-construction details). Reflectance spectra (figure 1a) were captured from representative patches using an OceanOptics USB4000-FL spectrometer and a PX-2 pulsed xenon light source, calibrated against a Spectralon (Labsphere, Congleton, UK) white standard. ...
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Much of what we know about human colour perception has come from psychophysical studies conducted in tightly-controlled laboratory settings. An enduring challenge, however, lies in extrapolating this knowledge to the noisy conditions that characterize our actual visual experience. Here we combine statistical models of visual perception with empirical data to explore how chromatic (hue/saturation) and achromatic (luminant) information underpins the detection and classification of stimuli in a complex forest environment. The data best support a simple linear model of stimulus detection as an additive function of both luminance and saturation contrast. The strength of each predictor is modest yet consistent across gross variation in viewing conditions, which accords with expectation based upon general primate psychophysics. Our findings implicate simple visual cues in the guidance of perception amidst natural noise, and highlight the potential for informing human vision via a fusion between psychophysical modelling and real-world behaviour.
... According to previous work, birds are the most likely selective agent driving phenotypic diversity in these and other poison frogs (e.g., refs. [28][29][30]. Thus, our results focus only on avian attacks, although it is worth noting that our models were also attacked by mammals and arthropods (SI Appendix, Fig. S2). ...
... While we did not observe white individuals in the yellow population, our results support the idea that if novel signals were to arise in the yellow population, they would be protected by the strong yellow signal. This possibility is supported by the existence of phenotypic polymorphism in some yellow populations of D. tinctorius, where a variety of patterns indicates that phenotype is not constrained (13), and that predators may indeed generalize among them (30). Interestingly, such color pattern variation in populations with white in their signals has never been reported. ...
... Avoidance Learning and Generalization. As avian predators are the likely drivers of aposematic signal evolution in D. tinctorius (29,30,63), we used a model avian predator, the domestic chicken (Gallus gallus domesticus), to assess how naïve predators learn and extend experience (generalize) with aposematic signals. Chickens are well-known for their capabilities of recognizing and learning different colors quickly (75), and thus widely used in this type of experiment (33,37,(76)(77)(78)(79). ...
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Aposematic organisms couple conspicuous warning signals with a secondary defense to deter predators from attacking. Novel signals of aposematic prey are expected to be selected against due to positive frequency-dependent selection. How, then, can novel phenotypes persist after they arise, and why do so many aposematic species exhibit intrapopulation signal variability? Using a polytypic poison frog (Dendrobates tinctorius), we explored the forces of selection on variable aposematic signals using 2 phenotypically distinct (white, yellow) populations. Contrary to expectations, local phenotype was not always better protected compared to novel phenotypes in either population; in the white population, the novel phenotype evoked greater avoidance in natural predators. Despite having a lower quantity of alkaloids, the skin extracts from yellow frogs provoked higher aversive reactions by birds than white frogs in the laboratory, although both populations differed from controls. Similarly, predators learned to avoid the yellow signal faster than the white signal, and generalized their learned avoidance of yellow but not white. We propose that signals that are easily learned and broadly generalized can protect rare, novel signals, and weak warning signals (i.e., signals with poor efficacy and/or poor defense) can persist when gene flow among populations, as in this case, is limited. This provides a mechanism for the persistence of intrapopulation aposematic variation, a likely precursor to polytypism and driver of speciation. aposematism | frequency-dependent selection | polymorphism | unpalatability | secondary defenses
... Local adaptation to specific environmental conditions that vary geographically can also maintain variation in warning signals. For example, specific colourations can be more efficient aposematic signals (Rojas, Rautiala, & Mappes, 2014) or optimize thermoregulation (Goulson, 1994;Hazel, 2002;Lindstedt, Lindström, & Mappes, 2008) or investment on immune defences (Nokelainen, Lindstedt, & Mappes, 2013) under certain habitat conditions. Furthermore, polytypism can be maintained by geographic variation in mate preferences (Kronforst et al., 2006;Maan & Cummings, 2009), or by differences in the interaction of local predator communities with different aposematic signals (divergent learning hypothesis; Chouteau & Angers, 2011, 2012Mallet & Barton, 1989;Nokelainen, Valkonen, Lindstedt, & Mappes, 2014;Noonan & Comeault, 2009;Valkonen et al., 2012). ...
... In addition, the distance between models was 1-1.5 m, following the ob- Models were left in the forest and collected after 6 days. Upon collection, we scored the presence of attack signals (e.g., scratches, F I G U R E 3 Projections of RGB scores of living frogs (filled symbols) and painted models (unfilled symbols) on the first two principal components of a PCA (a), and on a bi-dimensional colour space generated using a modification of Endler's (1990) teeth marks) and the identity of the attacker, which was assigned based on the marks left on models following Brodie (1993), Saporito et al. (2007, Hegna, Saporito, Gerow, andDonnelly (2011), Paluh, Hantak, andSaporito (2014), Rojas, Rautiala, et al. (2014) and Willink, García-Rodríguez, Bolaños, and Pröl (2014). Figure 4 shows examples of attacks scored as different predator types. ...
... Another important aspect is the environment where the signal is presented. Rojas et al. (2014) showed that signal detectability of the dyeing poison frog (Dendrobates tinctorius) depends on the light conditions under which signaling takes place. Thus, a range of conditions influence the attack risk of prey and further, sometimes predators may not act as predicted when their perception is evaluated through vision models. ...
... A geographic mosaic theory of coevolution (Thompson 1999) can predict that heterogeneous predator selection may facilitate multiple prey appearances (Rönkä et al. 2020). With this respect, variable light conditions have been identified as a potential source of heterogeneous selection that could result in the emergence of such phenotype variation (Rojas et al. 2014;Tate et al. 2016;Passarotto et al. 2018;Kranz et al. 2018). We found that predation risk on the different-colored A. plantaginis morphs was dependent on the light conditions that prey morphs and their predators were experiencing. ...
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A big question in behavioral ecology is what drives diversity of color signals. One possible explanation is that environmental conditions, such as light environment, may alter visual signaling of prey, which could affect predator decision-making. Here, we tested the context-dependent predator selection on prey coloration. In the first experiment, we tested detectability of artificial visual stimuli to blue tits (Cyanistes caeruleus) by manipulating stimulus luminance and chromatic context of the background. We expected the presence of the chromatic context to facilitate faster target detection. As expected, blue tits found targets on chromatic yellow background faster than on achromatic grey background whereas in the latter, targets were found with smaller contrast differences to the background. In the second experiment, we tested the effect of two light environments on the survival of aposematic, color polymorphic wood tiger moth (Arctia plantaginis). As luminance contrast should be more detectable than chromatic contrast in low light intensities, we expected birds, if they find the moths aversive, to avoid the white morph which is more conspicuous than the yellow morph in low light (and vice versa in bright light). Alternatively, birds may attack first moths that are more detectable. We found birds to attack yellow moths first in low light conditions, whereas white moths were attacked first more frequently in bright light conditions. Our results show that light environments affect predator foraging decisions, which may facilitate context-dependent selection on visual signals and diversity of prey phenotypes in the wild.
... As work in both this (F. Rezende, O. Nokelainen and J. Mappes, unpublished) and other (Rojas et al. 2014) species has shown that there can be an interaction between colour pattern and light environment on predator response, further research on the role of light environment on bird's perception of visual signals may shed further light on the apparent mismatch between different experimental set-ups. These findings suggest that detection at long distances may elicit a different response in predators (based purely on colour) than detection at short distances, where the effect of the repulsive odour produced by the methoxypyrazines (Guilford et al. 1987) plays a more significant role (see below). ...
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Allocation to different components of defence has been suggested as an explanation for the existence of multiple aposematic morphs in a single population. We tested whether there are trade-offs between warning colouration and chemical defence or whether these have an additive effect when combined, using blue tits (Cyanistes caeruleus) as predators and the polymorphic wood tiger moth (Arctia plantaginis) as prey. We used artificial edible models (with and without the moths’ defensive fluids) with paper wings whose colour and pattern properties matched those of real moths. When the models were presented sans defensive fluids or when the fluids were presented without colour cues, we detected no differences in initial avoidance between the two morphs. However, when the colour and chemical cues were combined, differences emerged. White wings elicited higher latency to approach regardless of the defensive fluids applied on them. After approach, however, the defensive fluids of both morphs presented on moth models elicited higher latency to attack than a water control, hinting at a repellent odour. Fluids of white moths rendered lower amounts of prey eaten regardless of wing colour, while yellow moths’ fluids provoked the highest occurrence of beak wiping behaviour. Our findings highlight the importance of accounting for interactive effects between different signal modalities, as these can create patterns not detectable when examined in isolation. Understanding these interactions is vital to determine how different components of multimodal warning displays provide protection at different stages of a predation event and, potentially, how multiple morphs can co-occur in a population. Significance statement There are many things that can stop a predator attacking a prey such as looking scary or smelling bad, but if a predator does take a bite, tasting bad can make the difference between life and death for the prey. When combined with bright conspicuous colours, both repellent odours and deterrent tastes (i.e. chemical defences) can help predators learn to avoid unprofitable prey. However, it is unclear whether it is really the sum of these visual and chemical signals that most effectively deters predators or whether one is more important than the other. Examining the effects of warning colour and chemical defence in white and yellow wood tiger moths on wild-caught birds, we show that neither aspect of the moths’ defence in isolation is as effective for predator deterrence as the sum of both.
... biologically relevant than color variation. Further, evidence that the detectability of different color pattern variants is influenced by the existing light environment(Rojas, Rautiala, & Mappes, 2014) underscores the importance of incorporating information on both predator sensory abilities and ambient lighting conditions into the characterization of phenotypic variation. Moving forward, it is important to determine which aspects of coloration and/or pattern are perceived by predators and conspecifics. ...
Article
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Intraspecific color variation has long fascinated evolutionary biologists. In species with bright warning coloration, phenotypic diversity is particularly compelling because many factors, including natural and sexual selection, contribute to intraspecific variation. To better understand the causes of dramatic phenotypic variation in Malagasy poison frogs, we quantified genetic structure and color and pattern variation across three closely related species, Mantella aurantiaca, Mantella crocea, and Mantella milotympanum. Although our restriction site‐associated DNA (RAD) sequencing approach identified clear genetic clusters, they do not align with current species designations, which has important conservation implications for these imperiled frogs. Moreover, our results suggest that levels of intraspecific color variation within this group have been overestimated, while species diversity has been underestimated. Within major genetic clusters, we observed distinct patterns of variation including: populations that are phenotypically similar yet genetically distinct, populations where phenotypic and genetic breaks coincide, and populations that are genetically similar but have high levels of within‐population phenotypic variation. We also detected admixture between two of the major genetic clusters. Our study suggests that several mechanisms—including hybridization, selection, and drift—are contributing to phenotypic diversity. Ultimately, our work underscores the need for a reevaluation of how polymorphic and polytypic populations and species are classified, especially in aposematic organisms.
... Additionally, thermoregulation and the effect of illumination on the signaler detectability may also influence perception (Rao and Mendoza-Cuenca 2016;Rojas et al. 2014). Furthermore, color vision models do not include other mechanisms, such as cognition, color categorization, past experiences, or memory imprecision (Renoult et al. 2015), even though these factors may affect detectability and, consequently, influence the survival rate of morphs differently (Théry and Gomez, 2010). ...
Article
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Color polymorphisms have been traditionally attributed to apostatic selection. The perception of color depends on the visual system of the observer. Theoretical models predict that differently perceived degrees of conspicuousness by two predator-prey species may cause the evolution of polymorphisms in the presence of anti-apostatic and apostatic selection. The spider Gasteracantha cancriformis (Araneidae) possesses several conspicuous color morphs. In orb-web spiders, the prey attraction hypothesis states that conspicuous colors are prey lures that increase spider foraging success via flower mimicry. Therefore, polymorphism could be maintained if each morph attracted a different prey species (multiple prey hypothesis) and each spider mimicked a different flower color (flower mimicry hypothesis). Conspicuous colors could be a warning signal to predators because of the spider’s hard abdomen and spines. Multiple predators could perceive morphs differently and exert different degrees of selective pressures (multiple predator hypothesis). We explored these three hypotheses using reflectance data and color vision modeling to estimate the chromatic and achromatic contrast of G. cancriformis morphs as perceived by several potential prey and predator taxa. Our results revealed that individual taxa perceive the conspicuousness of morphs differently. Therefore, the multiple prey hypothesis and, in part, the multiple predator hypothesis may explain the evolution of color polymorphism in G. cancriformis, even in the presence of anti-apostatic selection. The flower mimicry hypothesis received support by color metrics, but not by color vision models. Other parameters not evaluated by color vision models could also affect the perception of morphs and influence morph survival and polymorphism stability.
... In addition, sensory processing in the brain plays a role in determining key features influencing the effectiveness of warning signals, such as detectability, discriminability and memorability (Guilford & Dawkins, 1991). Finally, environmental conditions also affect the visibility and effectiveness of warning colours, dependent on ambient light and the characteristics of natural backgrounds (Endler, 1990(Endler, , 1993Bond & Kamil, 2006;Rojas, Rautiala & Mappes, 2014b); so aposematism overall, or some specific colour morphs, may be more effective in particular habitats. ...
Article
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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.
... Some amphibians have been shown to remain immobile in the presence of artificial light, which can further heighten predation risk (Mazerolle et al. 2005). Additionally, Rojas et al. (2014) found that avian predators attacked decoy frogs with more aposematic coloring less frequently in illuminated environments than more cryptically colored decoys. This could pose a threat to normally camouflaged wood frogs in artificial light conditions. ...
Article
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Light pollution is known to be problematic for many nocturnal organisms, but our understanding of its effects on amphibians is relatively poor. This is particularly true for recently metamorphosed, as their small size makes them difficult to track. Our objectives were to determine if wood frogs (Lithobates sylvaticus) and unisexual blue-spotted salamanders (Amybostoma laterale x jeffersonianum) select deciduous or coniferous leaf litter and if this behavior was affected by artificial light. We conducted choice experiments using 42 salamanders and 46 frogs placed in covered outdoor mesocosms. Each mesocosm was divided into half coniferous and half deciduous leaf litter and its underlying soil. Animals were given one night to choose a substrate, and their positions were recorded the next morning. We then conducted lighted trials in the same mesocosms, with a flashlight illuminating one substrate one night, and the other substrate the following night. Frogs did not have a leaf litter preference (p>0.20), and did not show a preference when either substrate was illuminated (p>0.20 with deciduous lit and 0.10
... Beyond questions addressing predator-prey interactions we advocate the use of clay models in visual detection experiments. Following Rojas et al. [23], who tested detection of models under different lighting conditions as well as different aposematic morphs, we deployed clay models to gain insights on detectability of prey with different morphological traits on different positions in the habitat using "human predators". In this kind of experiment the task is to spot models in the natural habitat to assess the importance of trait or habitat differences for human vision. ...
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Background: Many intriguing questions about predator-prey interactions can be addressed by using clay models of prey animals. These are placed in the field to test predators’ avoidances or preferences (testing e.g. color or shape) or to gain insights into predator identity. Modeling clay allows teeth, beak and jaw marks to remain on the model for identification. First used 30 years ago, clay models are now widely deployed. Ever since, the complexity of hypotheses, modeled species as well as the number of clay models used per study has increased. Although clay models are a valuable research tool, the method has limitations. Some questions cannot be addressed with these experiments, yet there is potential for improvement. Main body: We focus on the following aspects that need attention for clay model studies (CMS) in the future: (1) Use of proper clay materials, (2) how to standardize attack identification, (3) limitations of clay model studies, (4) use of clay models beyond predation experiments and (5) the next generation of clay model studies. Conclusion: We conclude that certain aspects of the clay model paradigm urgently need greater standardization. We advocate the use of harmless clay products and non-toxic inks, as well as having a neutral person to evaluate the marks left in the clay against pre-defined inclusion criteria. Further we suggest to use experimental data more cautiously in respect to evolutionary explanations, to use clay studies in detection experiments and to develop methods for attacker identification based on predator salivary DNA. Keywords: Ecological studies, Predator-prey interactions, Predator salivary DNA
... In the dyeing poison frog, Dendrobates tinctorius, an interplay between natural and sexual selection affecting warning signals has also been proposed, although in lesser detail. Field studies with frog models at Nouragues Reserve (French Guiana) have shown that the warning signals of D. tinctorius elicit few avian predator attacks (Noonan and Comeault, 2009;Rojas et al., 2014) and are subject, as expected, to positive frequencydependent selection (Comeault and Noonan, 2011). Males of this population have a higher proportion of yellow in their dorsal area than females, and the authors suggest that a synergy between sexual selection (in the form of parental care) and aposematism could select for yellower males (Rojas and Endler, 2013). ...
Article
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Chemically defended animals often display conspicuous color patterns that predators learn to associate with their unprofitability and subsequently avoid. Such animals (i.e., aposematic), deter predators by stimulating their visual and chemical sensory channels. Hence, aposematism is considered to be "multimodal." The evolution of warning signals (and to a lesser degree their accompanying chemical defenses) is fundamentally linked to natural selection by predators. Lately, however, increasing evidence also points to a role of sexual selection shaping warning signal evolution. One of the species in which this has been shown is the wood tiger moth, Arctia plantaginis, which we here put forward as a promising model to investigate multimodality in aposematic and sexual signaling. A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic coloration as well as sex-limited polymorphism in part of its range. The anti-predator function of its coloration and, more recently, its chemical defenses (even when experimentally decoupled from the visual signals), has been well-demonstrated. Interestingly, recent studies have revealed differences between the two male morphs in mating success, suggesting a role of coloration in mate choice or attraction, and providing a possible explanation for its sexual dimorphism in coloration. Here, we: (1) review the lines of evidence showing the role of predation pressure and sexual selection in the evolution of multimodal aposematic signals in general, and in the wood tiger moth in particular; (2) establish gaps in current research linking sexual selection and predation as selective pressures on aposematic signals by reviewing a sample of the literature published in the last 30 years; (3) highlight the need of identifying suitable systems to address simultaneously the effect of natural and sexual selection on multimodal aposematic signals; and (4) propose directions for future research to test how aposematic signals can evolve under natural and sexual selection.
... Further support for the role of poison frog colour patterns as an anti-predator strategy has been obtained in recent studies. Various field experiments have shown that colourful models representing local frogs are usually less frequently attacked than dull models, models representing novel morphs, or familiar models placed on novel backgrounds, at least for colours resembling the morphs of Oophaga pumilio in Costa Rica (Saporito et al., 2007b;Hegna et al., 2011;Stuart, Dappen & Losin, 2012) and Dendrobates tinctorius in French Guiana (Noonan & Comeault, 2009;Rojas, Rautiala & Mappes, 2014b). Interestingly, an experiment carried out in Isla Colón (Panamá) showed that the local, green morph of O. pumilio was attacked at significantly higher frequency than the foreign, red morph from the mainland (Hegna, Saporito & Donnelly, 2013). ...
Article
The role of colours and colour patterns in behavioural ecology has been extensively studied in a variety of contexts and taxa, while almost overlooked in many others. For decades anurans have been the focus of research on acoustic signalling due to the prominence of vocalisations in their communication. Much less attention has been paid to the enormous diversity of colours, colour patterns, and other types of putative visual signals exhibited by frogs. With the exception of some anecdotal observations and studies, the link between colour patterns and the behavioural and evolutionary ecology of anurans had not been addressed until approximately two decades ago. Since then, there has been ever-increasing interest in studying how colouration is tied to different aspects of frog behaviour, ecology and evolution. Here I review the literature on three different contexts in which frog colouration has been recently studied: predator–prey interactions, intraspecific communication, and habitat use; and I highlight those aspects that make frogs an excellent, yet understudied, group to examine the role of colour in the evolution of anti-predation strategies and animal communication systems. Further, I argue that in addition to natural-history observations, more experiments are needed in order to elucidate the functions of anuran colouration and the selective pressures involved in its diversity. To conclude, I encourage researchers to strengthen current experimental approaches, and suggest future directions that may broaden our current understanding of the adaptive value of anuran colour pattern diversity.
... Because of the increasing relevance of noise such as photon shot noise under dim light conditions, achromatic vision is likely a good option under such circumstances [34], and diurnal hawkmoths switch between achromatic and chromatic vision based on ambient illumination [35]. In general, it is now widely accepted that detectability changes with light conditions [36]. The consequences of this finding for vision-based features in night-blooming flowers must be explored. ...
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The night is a special niche characterized by dim light, lower temperatures, and higher humidity compared to the day. Several animals have made the transition from the day into the night and have acquired unique adaptations to cope with the challenges of performing nocturnal activities. Several plant species have opted to bloom at night, possibly as a response to aridity to prevent excessive water loss through evapotranspiration since flowering is often a water-demanding process, or to protect pollen from heat stress. Nocturnal pollinators have visual adaptations to function under dim light conditions but may also trade off vision against olfaction when they are dependent on nectar-rewarding and scented flowers. Nocturnal pollinators may use CO2and humidity cues emanating from freshly-opened flowers as indicators of nectar-rich resources. Some endothermic nocturnal insect pollinators are attracted to thermogenic flowers within which they remain to obtain heat as a reward to increase their energy budget. This review focuses on mechanisms that pollinators use to find flowers at night, and the signals that nocturnally blooming flowers may employ to attract pollinators under dim light conditions. It also indicates gaps in our knowledge. While millions of years of evolutionary time have given pollinators and plants solutions to the delivery of pollination services and to the offering of appropriate rewards, this history of successful evolution is being threatened by artificial light at night. Excessive and inappropriate illumination associated with anthropogenic activities has resulted in significant light pollution which serves to undermine life processes governed by dim light.
... The ancestrally 'black' clades gave rise to the 'yellow' pattern in Indo-Burma and Sumatra. The distinctiveness of the 'yellow' pattern is conditional 38 : these beetles are very conspicuous if sitting on the upper side of a leaf due to the high contrast 37 with dark green leaves under the tropical forest canopy. Conversely, they are much less conspicuous, at least to a human observer, if an individual sits on the bottom side and is observed against a clear sky (unpublished field observation). ...
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Multiple patterns and intraspecific polymorphism should not persist in mutualistic Müllerian systems due to purifying and frequency-dependent selection, but they are commonly identified in nature. We analysed molecular phylogeny and reconstructed dispersal history of 58 species of Dilophotes (Coleoptera: Lycidae) in Asia. Dilophotes colonized the Great Sundas and Malay Peninsula where they joined extensive mimetic communities of net-winged beetles. We identified the brightly bi-coloured males and females which adverged on five occasions to different autochthonous models. This is the first described case of Müllerian sexual dimorphism based on sex-specific body size. We propose that the constraint, i.e. the conservative sexual size dimorphism, forced the unprofitable prey to such complex adaptation in a multi-pattern environment. Although mimetic sexual dimorphism has frequently evolved in Dilophotes, a single pattern has been maintained by both sexes in multiple closely related, sympatrically occurring species. Some patterns may be suboptimal because they are rare, crudely resemble co-mimics, or are newly evolved, but they persist in Müllerian communities for a long time. We assume that failure to closely resemble the most common model can increase the diversity of large Müllerian communities and produce mimetic dimorphism.
... Am ezquita et al., 2013;Exnerov a et al., 2006;Gamberale & Tullberg, 1996;Gamberale-Stille & Tullberg, 1999;Ham et al., 2006;Rojas, Rautiala, & Mappes, 2014; ...
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Local warning colour polymorphism, frequently observed in aposematic organisms, is evolutionarily puzzling. This is because variation in aposematic signals is expected to be selected against due to predators' difficulties associating several signals with a given unprofitable prey. One possible explanation for the existence of such variation is predator generalization, which occurs when predators learn to avoid one form and consequently avoid other sufficiently similar forms, relaxing selection for monomorphic signals. We tested this hypothesis by exposing the three different colour morphs of the aposematic wood tiger moth, Arctia plantaginis, existing in Finland to local wild-caught predators (blue tits, Cyanistes caeruleus). We designed artificial moths that varied only in their hindwing coloration (white, yellow and red) keeping other traits (e.g. wing pattern and size) constant. Thus, if the birds transferred their aversion of one morph to the other two we could infer that their visual appearances are sufficiently similar for predator generalization to take place. We found that, surprisingly, birds showed no preference or aversion for any of the three morphs presented. During the avoidance learning trials, birds learned to avoid the red morph considerably faster than the white or yellow morphs, confirming previous findings on the efficacy of red as a warning signal that facilitates predator learning. Birds did not generalize their learned avoidance of one colour morph to the other two morphs, suggesting that they pay more attention to conspicuous wing coloration than other traits. Our results are in accordance with previous findings that coloration plays a key role during avoidance learning and generalization, which has important implications for the evolution of mimicry. We conclude that, in the case of wood tiger moths, predator generalization is unlikely to explain the unexpected coexistence of different morphs.
... There may also be local regional differences, presumably due to different communities of predators with different prior experience of apo- sematic prey (Carroll and Sherratt 2013;Exnerová et al. 2015). There may also be differences in the detectability of different pat- terns as a result of changes in the foliage canopy, height of the sun, weather and other factors affecting the light environment (Endler 1993;Rojas et al. 2014). These are all important factors to investi- gate in the future. ...
Article
Striped patterns are common in nature and are used both as warning signals and camouflage. Their effectiveness in either role depends on their color and spatial frequency, and how these compare to the background. Although this general principle is well established, the specific detail of how visual texture influences defensive coloration remains untested in the field. For aposematic patterns, especially, little work has focused on how pattern components, as opposed to color, affect warning signal efficacy. By presenting artificial moth-like stimuli, pinned to tree bark, to wild avian predators, and human observers, we examine how the spatial frequency and orientation of stripes affects the survival and detectability of yellow-and-black (aversive) and olive-and-black (cryptic) patterns. For the cryptic stripes, we find that matching the dominant spatial frequency and orientation of the background increases survival against bird predation and decreases the distance from which humans first detect the target. For aversive stripes, however, survival against birds peaked at spatial frequencies that neither matched the dominant background spatial frequency nor maximized the mismatch between target and background. This peak in survival at intermediate spatial frequencies did not match detectability by humans: There was no difference in the initial detection distance between stripes of different spatial frequencies, although the distance at which stripes could be resolved did differ. We suggest that, although the best cryptic strategy is to match the dominant components of the background as closely as possible, the optimal aposematic signal is one that balances signal distinctiveness and recognition at a distance.
... Other materials used are paraffin wax, plaster, and clay-covered plastic models (e.g. Stuart-Fox et al., 2003;Husak et al., 2006;Rojas, Rautiala & Mappes, 2014). Throughout this paper, we use the term modelling clay except where we specify the type of material used. ...
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We review the use of clay models to explore questions about predation rates on small vertebrate taxa that are typically difficult to observe directly. The use of models has a relatively long history and we examine the range of taxa studied, which includes squamate reptiles, amphibians, mammals and birds. Within this review, we have also included studies of model eggs, which are used in nest predation studies. We review the questions that have been asked and the interpretations arising from the data. The use of clay model animals has provided us with insights into how differences in prey morphology, size, and colour influence the rate at which they are attacked by predators. This allows us insights into the ecological, behavioural and evolutionary selective pressures of different predators on small vertebrate prey, including analysis of what characteristics predators target and how predators approach their prey (e.g. which part of the body is attacked). Further available interpretations include how regional and habitat variation influences predation events on models. We also briefly discuss the potential for clay models to study interspecific sociality and competition. Finally, we review the problems and limitations with the method and make some suggestions for further studies and amendments to help standardize this creative tool for ecological research.
... The results of our predation study show very low attack rates (of both brown and yellow model). However, due to the low sample size compared to similar studies (Saporito et al. 2007;Noonan and Comeault 2009;Hegna et al. 2011;Rojas et al. 2014), we cannot draw further conclusions regarding the costs of colour change. The marks left on the attacked models appeared to be teeth indents of rodents, which may be due to the materials used to make models rather than colour. ...
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Bright colouration appearing in one sex only can be driven by components of sexual selection including female choice, male competition or mate recognition. Male Litoria wilcoxii undergo rapid colour change from brown to yellow during amplexus, however, the function, if any, is unknown. We tested possible behavioural functions by observing breeding aggregations and behavioural responses (colour change, movement, call and amplexus duration) to varying stimuli (including model male and female frogs). We also examined whether colour change was a by-product of hormone release by comparing spermatic urine of frogs injected with epinephrine (colour change hormone) and hCG (triggers spermiation). Finally, the predation cost of being bright yellow was examined by placing frog models (yellow and brown) in the field and measuring predator attack rate. The behavioural responses of males to model females, brown/brown models (female with amplexing brown male), and brown/yellow models (female with amplexing yellow male), were similar to reactions towards real females, with the important exception that males did not attempt amplexus with brown/yellow models. Epinephrine injections triggered colour change but not sperm release in male frogs, while hCG induced sperm release but not colour change. Attack rates were low in predation trials with no difference in attack rates between yellow and brown models observed. Our study presents a novel function for rapid dynamic colour change as an intrasexual signal during amplexus that could avert sperm competition and displacement by other males. Significance statement Colour displays during breeding are believed to have evolved through mechanisms of sexual selection (female choice, male–male competition or sexual recognition). Stony creek frogs (Litoria wilcoxii) have been observed to rapidly change colour from brown (similar to female colouration) to bright yellow during amplexus, which is unusual as the colour change occurs after mate selection. Behavioural experiments were used to test hypotheses on the evolutionary function of colour change in this species. In L.wilcoxii, colour functions as an intrasexual signal during amplexus, we hypothesise that this could avert sperm competition and/or displacement by other males during amplexus. The function presented here is novel among amphibians, however as data on dynamic colour change in amphibians is lacking, this trait may be more common.
... Also, another study with wild birds showed that achromatic (non-coloured) Heliconius models were attacked significantly more than coloured models of a local pattern, demonstrating the importance of aposematic signals in avoiding predation (Finkbeiner et al., 2014). Furthermore, an experiment with model poison frogs [Dendrobates tinctorius (Schneider)] showed varying attack rates of wild tropical predators in different light conditions (Rojas et al., 2014). Still, few studies, to date, have explored attack rates on different coloured models using wild birds and under natural conditions. ...
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1. Birds are considered to be the primary selective agents for warning coloration in butterflies, and select for aposematic mimicry by learning to avoid brightly coloured prey after unpleasant experiences. It has long been thought that bright coloration plays an important role in promoting the avoidance of distasteful prey by birds. 2. We tested the hypothesis that warning colouration facilitates memorability and promotes predator avoidance by means of a field experiment using distasteful model butterflies. Artificial butterflies with a Heliconius colour pattern unknown to local birds were generated using bird vision models, either coloured or achromatic, and hung in tree branches in a tropical forest. Two sequential trials were conducted at each site in order to test avoidance by naïve and experienced predators. 3. There was a significant reduction in predation in the second trial. In addition, coloured models were attacked less than achromatic models. Specifically, coloured butterflies were attacked significantly less in the second trial, but there was no significant decrease in predation on achromatic models. 4. Our results imply an important role for colour in enhancing aversion of aposematic butterflies. We have also demonstrated that previous experience of distasteful prey can lead to enhanced avoidance in subsequent trials, supporting mimicry theory.
... For example, background complexity is an important factor contributing to an increased foraging effort [34][35][36][37]. In natural settings, the complex interplay of the light environment, background coloration, appearance and visual acuity will determine detection time and predation risk [18,[38][39][40][41][42] and ultimately shape anti-predator behaviours with light levels and background colours being a strong selective agent in birds. ...
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To avoid predation, many species rely on vision to detect predators and initiate an escape response. The ability to detect predators may be lower in darker light conditions or with darker backgrounds. For birds, however, this has never been experimentally tested. We test the hypothesis that the response time of avian prey (feral pigeon Columbia livia f. domestica) to a simulated hawk attack (taxidermy mounted colour-polymorphic black sparrowhawk Accipiter melanoleucus) will differ depending on light levels or background colour. We predict that response will be slower under darker conditions, which would translate into higher predation risk. The speed of response of prey in relation to light level or background colour may also interact with the colour of the predator, and this idea underpins a key hypothesis proposed for the maintenance of different colour morphs in polymorphic raptors. We therefore test whether the speed of reaction is influenced by the morph of the hawk (dark/light) in combination with light conditions (dull/bright), or background colours (black/white). We predict slowest responses to morphs under conditions that less contrast with the plumage of the hawk (e.g. light morph under bright light or white background). In support of our first hypothesis, pigeons reacted slower under duller light and with a black background. However, we found no support for the second hypothesis, with response times observed between the hawk-morphs being irrespective of light levels or background colour. Our findings experimentally confirm that birds detect avian predators less efficiently under darker conditions. These conditions, for example, might occur during early mornings or in dense forests, which could lead to changes in anti-predator behaviours. However, our results provide no support that different morphs may be maintained in a population due to differential selective advantages linked to improved hunting efficiencies in different conditions due to crypsis.
... As a result, an analysis that omitted the two attacks that were observed at night in Mexico (Fig. 5C) would provide a more robust test of how warning coloration factors into prey-selection decisions by predators. Similarly, because different color pattern phenotypes might vary in their conspicuousness to predators, differences in predation rates could be driven by both variation in prey preference and variation in visual detection rate (Stuart, Dappen & Losin, 2012;Rojas, Rautiala & Mappes, 2014). Variation in visual detection rate has been shown to be an unlikely explanation for differences in predation rates between color pattern phenotypes in at least a few aposematic taxa (Brodie, 1993;Wüster et al., 2004;Buasso, Leynaud & Cruz, 2006;McElroy, 2016). ...
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Artificial prey techniques—wherein synthetic replicas of real organisms are placed in natural habitats—are widely used to study predation in the field. We investigated the extent to which videography could provide additional information to such studies. As a part of studies on aposematism and mimicry of coral snakes ( Micrurus ) and their mimics, observational data from 109 artificial snake prey were collected from video-recording camera traps in three locations in the Americas ( terra firme forest, Tiputini Biodiversity Station, Ecuador; premontane wet forest, Nahá Reserve, Mexico; longleaf pine forest, Southeastern Coastal Plain, North Carolina, USA). During 1,536 camera days, a total of 268 observations of 20 putative snake predator species were recorded in the vicinity of artificial prey. Predators were observed to detect artificial prey 52 times, but only 21 attacks were recorded. Mammals were the most commonly recorded group of predators near replicas (243) and were responsible for most detections (48) and attacks (20). There was no difference between avian or mammalian predators in their probability of detecting replicas nor in their probability of attacking replicas after detecting them. Bite and beak marks left on clay replicas registered a higher ratio of avian:mammalian attacks than videos registered. Approximately 61.5% of artificial prey monitored with cameras remained undetected by predators throughout the duration of the experiments. Observational data collected from videos could provide more robust inferences on the relative fitness of different prey phenotypes, predator behavior, and the relative contribution of different predator species to selection on prey. However, we estimate that the level of predator activity necessary for the benefit of additional information that videos provide to be worth their financial costs is achieved in fewer than 20% of published artificial prey studies. Although we suggest future predation studies employing artificial prey to consider using videography as a tool to inspire new, more focused inquiry, the investment in camera traps is unlikely to be worth the expense for most artificial prey studies until the cost:benefit ratio decreases.
... These studies, however, largely focus on artificial targets presented against simple, unnatural backgrounds at close range, where the prey is always highly detectable. The impact of pattern on detectability can, however, also depend on context and viewing distance (Tullberg et al. 2005;Bohlin et al. 2012;Rojas et al. 2014;Honma et al. 2015;Barnett et al. 2018). Despite the apparent high internal contrast of the three color patterns we examined here, there was no evidence of disruptive camouflage in any of our frogs. ...
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Animals use color both to conceal and signal their presence, with patterns that match the background, disrupt shape recognition, or highlight features important for communication. The forms that these color patterns take are responses to the visual systems that observe them and the environments within which they are viewed. Increasingly, however, these environments are being affected by human activity. We studied how pattern characteristics and habitat change may affect the detectability of three frog color patterns from the Bocas del Toro archipelago in Panama: Beige-Striped Brown Allobates talamancae and two spotted morphs of Oophaga pumilio, Black-Spotted Green and Black-Spotted Red. To assess detectability, we used visual modeling of conspecifics and potential predators, along with a computer-based detection experiment with human participants. Although we found no evidence for disruptive camouflage, we did find clear evidence that A. talamancae stripes are inherently more cryptic than O. pumilio spots regardless of color. We found no evidence that color pattern polytypism in O. pumilio is related to differences in the forest floor between natural sites. We did, however, find strong evidence that human disturbance affects the visual environment and modifies absolute and rank order frog detectability. Human-induced environmental change reduces the effectiveness of camouflage in A. talamancae, reduces detectability of Black-Spotted Green O. pumilio, and increases chromatic contrast, but not detectability, in Black-Spotted Red O. pumilio. Insofar as predators may learn about prey defenses and make foraging decisions based on relative prey availability and suitability, such changes may have wider implications for predator–prey dynamics.
... The combination of conspicuous coloration and toxicity is an effective defense mechanism because predators learn to associate unpalatability with bright color patterns (Mappes et al. 2005). Such aversion learning is achieved at a faster rate when aposematic signals are more conspicuous and are thereby easier to detect and remember Endler and Mappes 2004;Mappes et al. 2005;Rojas et al. 2014Rojas et al. , 2015. When viewed dorsally, P. vittatus has a contrasting color pattern. ...
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Frogs in the genus Phyllobates are known for the presence of batrachotoxin, a highly toxic alkaloid, in their skin. Nevertheless, Phyllobates frogs from Costa Rica and Panama (P. lugubris and P. vittatus) are considered non-toxic, as they have been reported to harbor low concentrations of this alkaloid. However, the potential toxicity of Central American Phyllobates has not been assessed experimentally. Our goal was to determine the toxicity of the whole skin of P. vittatus, an endemic species from the Southeastern Pacific region of Costa Rica. We performed median lethal dose (LD 50) tests in mice to determine general toxicity, and an irritant assay based on the behavioral responses of mice to subcutaneous injection, to determine differences in irritability, as a measure of toxicity, among three study localities. Using UPLC-ESI-QTOF, we obtained chemical profiles of the methanolic extract of frog skins. Due to the absence of mortality at the studied doses, we were unable to estimate LD 50. However, we recorded a list of toxicity symptoms in mice that are consistent with cardiotoxic effects, and found that mice presented more symptoms at higher concentrations of skin extracts during the first hour of the LD 50 assays, recovering completely at all doses by the end of the assay. On the other hand, we did not detect differences in irritability among studied localities. Additionally, we putatively identified three toxic alkaloids (Batrachotoxinin A, DHQ 251A and Lehm 275A). This study provides the first experimental data on the toxicity and associated symptoms in mice, as well as the chemical profile of the skin of P. vittatus. We suggest that the skin alkaloids of P. vitattus may confer a chemical defense towards predators.
... Hexokinase (spot 2) is involved in carbohydrate metabolism as reported in Arabidopsis, and it converts phosphorylate glucose to glucose-6-phosphate, the first step in the glucose metabolic pathway (Karve et al. 2008). The present findings are in conformity with Rojas et al. (2014) who painted a new perspective of the relevance of primary metabolism in regulating the plant defense mechanism against pathogens. ...
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Main conclusion Induced mutagenesis using embryogenic cell suspension (ECS) explants with toxin based screening is an effective tool to create non-chimeral Fusarium wilt resistant mutants in banana. Global proteomics unravel the molecular mechanism behind resistance. Abstract Race 1 of Fusarium wilt is a serious threat to Musa spp. cv.Rasthali (AAB, Silk subgroup) which is a choice variety traditionally grown in most of the south East Asian countries. Resistant gene introgression into susceptible varieties through conventional breeding has several limitations and the predominant ones being sterility and long generation time. Under such circumstances, induced mutagenesis combined with toxin based in vitro screening remains as the viable alternative for the development of fusarium wilt resistant Rasthali. Therefore, induced mutagenesis was attempted by using ethylmethane sulfonate (EMS) in embryogenic cell suspension (ECS) of Rasthali followed by in vitro screening for fusarium wilt resistance using new generation toxins and pot screening through challenge inoculation with Foc race 1. This ultimately resulted in the identification of 15 resistant lines. Global proteomic analysis in one of the resistant mutant lines namely NRCBRM15 and its wild type revealed 37 proteins, of which 20 showed differential expression. Out of 20 proteins, nineteen were significantly abundant in NRCBRM15 and only one was abundant in wild Rasthali. A total of nine genes based on protein expression were further validated using quantitative real time polymerase chain reaction (qRT-PCR). Annotation results revealed that some of the genes namely Enolase, ATP synthase-alpha subunit, Actin 2, Actin 3,—glucanase, UTP-glucose-1-phosphate uridylyltransferase, Respiratory burst oxidase homolog, V type proton ATPase catalytic subunit A and DUF292 domain containing protein are involved in diverse functions such as carbohydrate metabolism, energy production, electron carrier, response to wounding, binding proteins, cytoskeleton organization, extracellular region, structural molecule and defense.
... They can influence intraspecific variation in mating cues (Merrill et al., 2012;Nokelainen et al., 2012), fitness of colour morphs in different light environments due to increased predation risk Rojas et al., 2014) and divergence in thermoregulatory capabilities (Forsman, 2000;Hegna et al., 2013;Lindstedt et al., 2009). As it has become possible to model the conspicuousness of different genotypes to different receivers (Endler & Basolo, 1998;Hart, 2001a;Henze et al., 2018), we may soon be able to estimate how their appearance shapes the fate of allelic combinations using long-term data sets (Le Rouzic et al., 2015;Svensson & Abbott, 2005). ...
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The definition of colour polymorphism is intuitive: genetic variants express discretely coloured phenotypes. This classification is, however, elusive as humans form subjective categories or ignore differences that cannot be seen by human eyes. We demonstrate an example of a 'cryptic morph' in a polymorphic wood tiger moth (Arctia plantaginis), a phenomenon that may be common among well-studied species. We used pedigree data from nearly 20,000 individuals to infer the inheritance of hindwing colouration. The evidence supports a single Mendelian locus with two alleles in males: WW and Wy produce the white and yy the yellow hindwing colour. The inheritance could not be resolved in females as their hindwing colour varies continuously with no clear link with male genotypes. Next, we investigated if the male genotype can be predicted from their phenotype by machine learning algorithms and by human observers. Linear discriminant analysis grouped male genotypes with 97% accuracy, whereas humans could only group the yy genotype. Using vision modelling, we also tested whether the genotypes have differential discriminability to humans, moth conspecifics and their bird predators. The human perception was poor separating the genotypes, but avian and moth vision models with ultraviolet sensitivity could separate white WW and Wy males. We emphasize the importance of objective methodology when studying colour polymorphism. Our findings indicate that by-eye categorization methods may be problematic, because humans fail to see differences that can be visible for relevant receivers. Ultimately, receivers equipped with different perception than ours may impose selection to morphs hidden from human sight.
... They can influence intraspecific variation in mating cues (Merrill et al., 2012;Nokelainen et al., 2012), fitness of colour morphs in different light environments due to increased predation risk Rojas et al., 2014) and divergence in thermoregulatory capabilities (Forsman, 2000;Hegna et al., 2013;Lindstedt et al., 2009). As it has become possible to model the conspicuousness of different genotypes to different receivers (Endler & Basolo, 1998;Hart, 2001a;Henze et al., 2018), we may soon be able to estimate how their appearance shapes the fate of allelic combinations using long-term data sets (Le Rouzic et al., 2015;Svensson & Abbott, 2005). ...
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Phenotypic variation is suggested to facilitate the persistence of environmentally growing pathogens under environmental change. Here we hypothesized that the intensive farming environment induces higher phenotypic variation in microbial pathogens than natural environment, because of high stochasticity for growth and stronger survival selection compared to the natural environment. We tested the hypothesis with an opportunistic fish pathogen Flavobacterium columnare isolated either from fish farms or from natural waters. We measured growth parameters of two morphotypes from all isolates in different resource concentrations and two temperatures relevant for the occurrence of disease epidemics at farms and tested their virulence using a zebrafish (Danio rerio) infection model. According to our hypothesis, isolates originating from the fish farms had higher phenotypic variation in growth between the morphotypes than the isolates from natural waters. The difference was more pronounced in higher resource concentrations and the higher temperature, suggesting that phenotypic variation is driven by the exploitation of increased outside‐host resources at farms. Phenotypic variation of virulence was not observed based on isolate origin but only based on morphotype. However, when in contact with the larger fish, the less virulent morphotype of some of the isolates also had high virulence. As the less virulent morphotype also had higher growth rate in outside‐host resources, the results suggest that both morphotypes can contribute to F. columnare epidemics at fish farms, especially with current prospects of warming temperatures. Our results suggest that higher phenotypic variation per se does not lead to higher virulence, but that environmental conditions at fish farms could select isolates with high phenotypic variation in bacterial population and hence affect evolution in F. columnare at fish farms. Our results highlight the multifaceted effects of human‐induced environmental alterations in shaping epidemiology and evolution in microbial pathogens.
... To quantify model salamander detectability, we conducted a detectability experiment where human participants (n = 22) searched a 20 × 20m grid (10 min) for our models (see Supplementary Material). We acknowledge the difference in visual capacity between human observers and wild predators, but contend that this work provides at least a coarse assessment of detectability differences among model treatments (e.g., see also Rojas et al. 2014;Rößler et al. 2019). Moreover, all model types were identical in color, so differences color-vision among predator types should minimally affect treatment-related differences in detectability for a given predator. ...
Article
A wide variety of prey use defensive postures as a means of protection from predators. Many salamanders engage in broadly similar defensive postures, which may function as a warning signal and reduce the probability of attack, or may deflect predator attacks away from vital body parts. The extent to which these strategies (i.e., aposematism and deflection) act exclusively or synergistically, however, remains unknown. We deployed clay salamanders in the field, manipulating size (small, large) and posture (resting, defensive), and documented attack rates across three predator types. Competing risks analysis revealed that attack rates were affected by model size, deployment period, and leaf litter depth at the site of deployment, whereas model posture had no significant effect. Model size and posture did not interact, indicating that defensive posture was ineffective in deterring attack irrespective of prey size. Model prey in the defensive posture received significantly more attacks on the tail irrespective of size, and the defensive posture was more effective at deflecting avian attacks compared to mammal predation. We conclude that defensive posture increases tail conspicuousness without increasing predation risk, and primarily functions to deflect attacks away from vital body parts. The efficacy of defection may be further increased by tail undulation, however our use of static models means that we cannot exclude aposematic or deimatic functions for such movements. Our results provide important support for the deflection hypothesis in explaining antipredator behavior, and thereby set the stage for additional research targeting the functionality of attack deflection in natural predator–prey encounters.
... Additional experiments are needed to determine the interactive effects of predator's generalization, larval group size, larval defensive displays, and color. To assess whether predation risk for yellow-and white-bodied larvae varies among N. lecontei populations, future research should also test for differences in the survival of white-and yellow-bodied larvae across their geographical range and across different visual backgrounds (Rojas et al. 2014;Rönkä et al. 2020). ...
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Our understanding of how novel warning color traits evolve in natural populations is largely based on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency‐dependent predation and positive assortative mating. Here, we integrate data from field surveys, predation experiments, population genomics, and phenotypic correlations to explain the origin and maintenance of geographic variation in a diet‐based larval pigmentation trait in the redheaded pine sawfly (Neodiprion lecontei), a pine‐feeding hymenopteran. Although our experiments confirm that N. lecontei larvae are indeed aposematic—and therefore likely to experience frequency‐dependent predation—our genomic data do not support a historical demographic scenario that would have facilitated the spread of an initially deleterious allele via drift. Additionally, significantly elevated differentiation at a known color locus suggests that geographic variation in larval color is currently maintained by selection. Together, these data suggest that the novel white morph likely spread via selection. However, white body color does not enhance aposematic displays, nor is it correlated with enhanced chemical defense or immune function. Instead, the derived white‐bodied morph is disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts, suggesting that bottom‐up selection via host plants may have driven divergence among populations. Overall, our results suggest that life stage and pigment source can have a substantial impact the evolution of novel warning signals, highlighting the need to investigate diverse aposematic taxa to develop a comprehensive understanding of color variation in nature. This article is protected by copyright. All rights reserved
... Previous studies showed that body size (Remmel and Tammaru 2009, Moura et al. 2018, Sahayaraj and Fernandez 2021, coloration (Théry and Gomez 2010, Zvereva et al. 2019, Aslam et al. 2020, and shape (Paluh et al. 2015) could influence the behavior of arthropod predators and how they interact with clay models. Additionally, predation rates can vary and could be subject to the difference in the appearance of prey or the reflectance of light from the model (Rojas et al. 2014, Cheng et al. 2018. However, the effects of the characteristics of the clay model, such as color, size, and shape, on arthropod predator interactions are not documented in turfgrass field settings. ...
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Many predatory arthropods occur naturally in turfgrass, and they provide adequate control of lepidopteran pests, such as fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae), and black cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae). Recording predation is challenging under field conditions because predators rarely leave any evidence. Clay models were successfully employed for studying predation, and this technique is underutilized in turfgrass. Little is known about whether the characteristics of clay models, such as color, shape, and size, influence arthropod interactions in turfgrass. To improve the utility of clay models in turfgrass, the influence of the color, shape, and size of clay models on arthropod interactions was studied by exposing clay models during daytime and nighttime in a turfgrass field. The results showed that arthropods interacted with clay models, and various types of impressions were recorded, including paired marks, scratches, cuts, and pricks. Although the color of the clay model had no significant effects on arthropod interactions during the night, significantly greater numbers of impressions were noticed on the blue and green models than on the yellow models during the daytime. The caterpillar-shaped models captured significantly greater densities of impressions than the beetle-shaped models. Additionally, the number of impressions significantly increased with an increase in the size of the model regardless of shape.
... For instance, the light environment may modify the conspicuousness of colour patterns (Rojas et al., 2014) Although we cannot rule out that an unidentified local selection might promote the evolution of a similar colour pattern in the three species, the observed repeated local convergence is also consistent with the escape mimicry hypothesis. In Müllerian mimetic species such as the butterfly species Heliconius melpomene and H. erato, multiple geographic races with striking colour pattern variations are maintained within species, with strong resemblance to races from the other species (Jiggins, 2017). ...
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Species interactions such as mimicry can promote trait convergence but disentangling this effect from those of shared ecology, evolutionary history and niche conservatism is often challenging. Here by focusing on wing color pattern variation within and between three butterfly species living in sympatry in a large proportion of their range, we tested the effect of species interactions on trait diversification. These butterflies display a conspicuous iridescent blue coloration on the dorsal side of their wings and a cryptic brownish colour on the ventral side. Combined with an erratic and fast flight, these color patterns increase the difficulty of capture by predators and contribute to the high escape abilities of these butterflies. We hypothesize that, beyond their direct contribution to predator escape, these wing patterns can be used as signals of escape abilities by predators, resulting in positive frequency-dependent selection favouring convergence in wing pattern in sympatry. To test this hypothesis, we quantified dorsal wing pattern variations of 723 butterflies from the three species sampled throughout their distribution, including sympatric and allopatric situations and compared the phenotypic distances between species, sex and localities. We detected a significant effect of localities on colour pattern, and higher inter-specific resemblance in sympatry as compared to allopatry, consistent with the hypothesis of local convergence of wing patterns. Our results provide support to the existence of escape mimicry in the wild and stress the importance of estimating trait variation within species to understand trait variation between species, and to a larger extent, trait diversification at the macro-evolutionary scale.
... Colour polymorphisms could also have evolved as aposematic signals in response to different predator species (Briolat et al., 2019). Polymorphisms may be favoured in situations where lighting conditions vary which favour different colour morphs (Rojas, Rautiala & Mappes, 2014). ...
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The strategies underlying different forms of protective coloration are well understood but little attention has been paid to the ecological, life-history and behavioural circumstances under which they evolve. While some comparative studies have investigated the ecological correlates of aposematism, and background matching, the latter particularly in mammals, few have examined the ecological correlates of other types of protective coloration. Here, we first outline which types of defensive coloration strategies may be exhibited by the same individual; concluding that many protective coloration mechanisms can be employed simultaneously, particularly in conjunction with background matching. Second, we review the ecological predictions that have been made for each sort of protective coloration mechanism before systematically surveying phylogenetically controlled comparative studies linking ecological and social variables to antipredator defences that involve coloration. We find that some a priori predictions based on small-scale empirical studies and logical arguments are indeed supported by comparative data, especially in relation to how illumination affects both background matching and self-shadow concealment through countershading; how body size is associated with countershading, motion dazzle, flash coloration and aposematism, although only in selected taxa; how immobility may promote background matching in ambush predators; and how mobility may facilitate motion dazzle. Examination of nearly 120 comparative tests reveals that many focus on ecological variables that have little to do with predictions derived from antipredator defence theory, and that broad-scale ecological studies of defence strategies that incorporate phylogenetics are still very much in their infancy. We close by making recommendations for future evolutionary ecological research.
... A teoria do impulso sensorial vem sendo apoiada por um corpo crescente de evidências, sugerindo que seleção do sinal depende do micro-habitat que o sinal é emitido (Chunco et al., 2007;Stuart-Fox et al., 2007;Rojas et al., 2014;White & Kemp, 2016 (Maan & Cummings, 2011;Dell'Aglio et al., 2018) com exceção dos mamíferos que são por maioria dicromático (Vorobyev & Osorio, 1998 Burtt Jr, 1979), ou refletir o espectro das machas solares que adentram a floresta (laranja-vermelho) são as melhores estratégias (Endler, 1992(Endler, , 1993. Portanto, a seleção teoricamente favoreceria a intensidade da cor, com animais de coloração escura em contraste a ambientes claros e simplescomo desertos e áreas abertas -e animais com cores contrastantes com o ambiente em habitats mais complexoscomo florestas (Endler, 1992). ...
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Color can play multiple roles in the lives of animals, from thermoregulation to protection against damage from ultraviolet radiation, aposematism, camouflage and sexual attraction. Because these traits depend on the physiology of the animal, color patterns are highly influenced by the environmental conditions in which the species are distributed, thus varying throughout their distribution. Studies on the variations of these features over different geographic gradients are, therefore, fundamental for a better understanding of the ecological and evolutionary processes that shape animal coloration. Females of Mutillidae wasps (velvet-ants) have striking color patterns that are recognized as aposematic signals, forming one of the largest mimetic rings in the Animal Kingdom. However, the causes underlying the evolution of these color patterns remain uncertain, since Müllerian and Batesian mimicry may not be the only selective forces behind aposematic color. Therefore, in the present study, we seek to elucidate whether coloration in velvet-ants responds to bioclimatic variations, testing three ecogeographic rules: The Thermal Melanism hypothesis; the Photoprotection hypothesis; and Gloger's rule. For this, we used photographs of 511 specimens of female Mutillidae wasps distributed in 21 countries and extracted data on the color in the form of the HSV color channels. Finally, we analyzed whether the variation in color observed is determined by bioclimatic factors, considering the phylogenetic signal: temperature, solar radiation, humidity, and environments with low light. Our results were consistent with the Photoprotection hypothesis and Gloger's rule. Species with darker coloration occupied habitats with more vegetation, higher humidity, and solar radiation. Darker animals also occurred in warmer environments, suggesting that Mutillidae do not respond to the predictions of the Thermal Melanism hypothesis. Our results also suggest that, in forest environments, velvet-ants have lower color saturation and heterogeneity. Females with more reddish and heterogeneous color occupied more open habitats. The results presented here provide the first evidence that abiotic components of the environment can act as ecological filters and selective forces on the coloration patterns in velvet-ants. Finally, we suggest that studies using Mutillidae as a model for mimetic complexes consider that mimicry may also be under the influence of climatic factors and not only predators
... Therefore, variation in the illumination regime, both between and within habitats, may cause considerable differences in predation rates on the same kind of prey. For example, predation intensity on the same object can differ between illuminated and shady environments (Cheng et al., 2018;Rojas, Rautiala, & Mappes, 2014), and variations in ultraviolet light may considerably affect the search behavior of insectivorous birds (Church, Bennett, Cuthill, & Partridge, 1998). ...
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... However, laboratory experiments have some limitations when extrapolated to natural conditions, because many environmental factors can affect the outcome of selection on prey colouration. In particular, natural variations in background characteristics and illumination can influence the responses of individual predators to prey colouration (Endler 1993;Rojas et al. 2014;Théry and Gomez 2010), potentially leading to spatial variations in selection pressure. ...
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Descriptive studies of natural history have always been a source of knowledge on which experimental work and scientific progress rely. Poison frogs are a well-studied group of small Neotropical frogs with diverse parental behaviors, distinct calls, and bright colors that warn predators about their toxicity; and a showcase of advances in fundamental biology through natural history observations. The dyeing poison frog, Dendrobates tinctorius , is emblematic of the Guianas region, widespread in the pet trade, and increasingly popular in research. This species shows several unusual behaviors, such as the lack of advertisement calls and the aggregation around tree-fall gaps, which remain poorly described and understood. Here, we summarize our observations from a natural population of D. tinctorius in French Guiana collected over various field trips between 2009 and 2017; our aim is to provide groundwork for future fundamental and applied research spanning parental care, animal dispersal, disease spread, habitat use in relation to color patterns, and intra-specific communication, to name a few. We report sex differences in habitat use and the striking invasion of tree-fall gaps; describe their courtship and aggressive behaviors; document egg development and tadpole transport; and discuss how the knowledge generated by this study could set the grounds for further research on the behavior, ecology, and conservation of this species.
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Selection for signal efficacy in variable environments may favour colour polymorphism, but little is known about this possibility outside of sexual systems. Here we used the colour polymorphic orb-web spider Gasteracantha fornicata, whose yellow- or white-banded dorsal signal attracts dipteran prey, to test the hypothesis that morphs may be tuned to optimize either chromatic or achromatic conspicuousness in their visually noisy forest environments. We used data from extensive observations of naturally occurring spiders and precise assessments of visual environments to model signal conspicuousness according to dipteran vision. Modelling supported a distinct bias in the chromatic (yellow morph) or achromatic (white morph) contrast presented by spiders at the times when they caught prey, as opposed to all other times at which they may be viewed. Hence, yellow spiders were most successful when their signal produced maximum colour contrast against viewing backgrounds, whereas white spiders were most successful when they presented relatively greatest luminance contrast. Further modelling across a hypothetical range of lure variation confirmed that yellow-versus-white signals should respectively enhance chromatic-versus-achromatic conspicuousness to flies, in G. fornicata's visual environments. These findings suggest that colour polymorphism may be adaptively maintained by selection for conspicuousness within different visual channels in receivers. This article is protected by copyright. All rights reserved.
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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 Heliconius butterflies, which occupy different habitats (open-canopy vs. closed-canopy), and one palatable, cryptic, generalist species Junonia coenia. 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.
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Biologists have reported on the chemical defences and the phenetic similarity of net-winged beetles (Coleoptera: Lycidae) and their co-mimics. Nevertheless, our knowledge has remained fragmental, and the evolution of mimetic patterns has not been studied in the phylogenetic context. We illustrate the general appearance of ~ 600 lycid species and ~ 200 co-mimics and their distribution. Further, we assemble the phylogeny using the transcriptomic backbone and ~ 570 species. Using phylogenetic information, we closely scrutinise the relationships among aposematically coloured species, the worldwide diversity, and the distribution of aposematic patterns. The emitted visual signals differ in conspicuousness. The uniform coloured dorsum is ancestral and was followed by the evolution of bicoloured forms. The mottled patterns, i.e. fasciate, striate, punctate, and reticulate, originated later in the course of evolution. The highest number of sympatrically occurring patterns was recovered in New Guinea and the Andean mountain ecosystems (the areas of the highest abundance), and in continental South East Asia (an area of moderate abundance but high in phylogenetic diversity). Consequently, a large number of co-existing aposematic patterns in a single region and/or locality is the rule, in contrast with the theoretical prediction, and predators do not face a simple model-like choice but cope with complex mimetic communities. Lycids display an ancestral aposematic signal even though they sympatrically occur with differently coloured unprofitable relatives. We show that the highly conspicuous patterns evolve within communities predominantly formed by less conspicuous Müllerian mimics and, and often only a single species displays a novel pattern. Our work is a forerunner to the detailed research into the aposematic signalling of net-winged beetles.
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Parental care is remarkably and widespread among vertebrates because of its clear fitness benefits. Caring however incurs energetic and ecological costs including increasing predation risk. Anurans have diverse forms of parental care, and we test whether the evolution of care is associated with morphology that minimizes predation risk. Specifically, we determine whether dichromatism, specific colours gradients, and patterns that enhance crypticity are associated with anurans that also evolve parental care. From our phylogenetic comparative analyses of 988 anurans distributed globally, we find that parental care is less likely to evolve in species with dichromatism. Contrary to our expectation, specific colours (Green-Brown, Red-Blue-Black, Yellow) and patterns (Plain, Spots, Mottled-Patches) were not associated with the evolution of caregiving behaviours. Only among species with male-only care did we find a positive association with the presence of Bars-Bands. The lack of strong associations between dorsal morphology and caregiving activities suggest that these colours and patterns may serve other functions and that predation risk of parental care is mediated in other ways. As a strongly sexually selected trait, dichromatism is an effective solution to attract mates, but we find here that its evolution appears to preclude the evolution of parental care behaviour in anurans.
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A few colors, such as red and yellow, are commonly found in aposematic (warning) signaling across taxa, independent of evolutionary relationships. These colors have unique traits (i.e., hue, brightness) that aid in their differentiation, and perhaps, their effectiveness in promoting avoidance learning. This repeated use calls into question the influence of selection on specific warning colors adopted by aposematic prey-predator systems. To disentangle the influence of color characteristics on this process, we trained week-old chickens (Gallus gallus domesticus) to learn to avoid distasteful food that was associated with one of three color signals (yellow, white, red) that varied in both hue and in brightness in order to assess which of these traits most influenced their ability to learn avoidance. Our results show that while chicks learned to avoid all three colors, avoidance was based on the hue, not brightness of the different signals. We found that yellow was the most effective for avoidance learning, followed by red, and finally white. Our results suggest that while these three colors are commonly used in aposematic signaling, predators' ability to learn avoidance differs among them. These results may explain why yellow is among the most common signals across aposematic taxa.
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Anti-predator signaling is highly variable with numerous examples of species employing cryptic coloration to avoid detection or conspicuous coloration (often coupled with a secondary defense) to ensure detection and recollection. While the ends of this spectrum are clear in their function, how species use intermediate signals is less clear. Australian Brood Frogs (Pseudophryne) display conspicuous coloration on both their dorsum and venter. Coupled with the alkaloid toxins these frogs possess, this coloration may be aposematic, providing a protective warning signal to predators. We assessed predation rates of known and novel color patterns and found no difference for avian or mammalian predators. However, when Pseudophryne dorsal phenotypes were collectively compared to the high-contrast ventral phenotype of this genus, we found birds, but not mammals, attacked dorsal phenotypes significantly less frequently than the ventral phenotype. This study, importantly, shows a differential predator response to ventral coloration in this genus which has implications for the evolution of conspicuous signaling in Pseudophryne.
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Our understanding of how novel color traits evolve in aposematic taxa is based largely on studies of reproductive stages and organisms with endogenously produced pigmentation. In these systems, genetic drift is often required for novel alleles to overcome strong purifying selection stemming from frequency-dependent predation and positive assortative mating. Here we show that the importance of these mechanisms can differ if selective processes are considered in larval stage instead. By integrating population genomic data, predation experiments and phenotypic measurements of larvae and their host plants, we show that novel white alleles in Neodiprion lecontei (pine sawfly) larvae spread via selection rather than drift. The cost of being rare was not offset by an enhanced aposematic display or immune function. Instead, bottom-up selection via host plants may drive divergence among populations as white larvae were disproportionately abundant on a pine species with a reduced carotenoid content relative to other pine hosts.
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Forests are a mosaic of light spectra, and colour signal efficiency might change in different light environments. Local adaptation in Heliconius butterflies is linked to microhabitat use and the colourful wing colour patterns may be adapted for signalling in different light environments. These toxic butterflies exhibit conspicuous colours as a warning to predators that they should be avoided, but also find and choose potential mates based on colour signals. The two selection pressures of predation and mate preference are therefore acting together. Colour conspicuousness should show habitat-specific contrast for the butterflies, which would facilitate detection and species identification. On the other hand, selection for signal stability would be stronger in the avian visual system. In this study we analysed the contrast of two Heliconius mimicry rings in their natural habitats under varying degrees of forest fragmentation and light conditions. We used digital image analyses and mapped the bird and butterfly vision colour space in order to examine whether warning colours have greater contrast and if they transmit a consistent signal across time of the day and habitat in a tropical forest. We tested conspicuousness using opponent colour channels against a natural green background. For avian vision, colours are generally very stable through time and habitat. For butterfly vision, there is some evidence that species are more contrasting in their own habitats, where conspicuousness is higher for red and yellow bands in the border and for white in the forest. Light environment affects Heliconius butterflies’ warning signal transmission to a higher degree through their own vision, but to a lesser degree through avian predator vision. This work provides insight into the use of colour signals in sexual and natural selection in the light of ecological adaptation.
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Anti-predator strategies can influence trade-offs governing other activities important to fitness. Crypsis, for example, might make conspicuous sexual display especially costly, whereas aposematism might reduce or remove such costs. We tested for correlates of anti-predator strategy in Oophaga pumilio, a polytypic poison frog with morphs spanning the crypsis–aposematism continuum. In the wild, males of visually conspicuous morphs display from conspicuous perches and behave as if they perceive predation risk to be low. We thus predicted that, given a choice of ambient light microhabitats, these males would use high ambient light conditions the most and be most likely to perch in high-light conditions. We found no evidence that differently colored male O. pumilio preferentially used bright microhabitats or that ambient light influenced perching in a morph-specific manner. Independent of light conditions, males from the most conspicuous population perched the least, but the most conspicuous individuals from a polymorphic population perched the most. These patterns suggest that preferences do not necessarily underlie among-morph differences observed in the wild. This could be explained, and remain consistent with theory, if risk aversion is shaped, in part, by experience.
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Müllerian mimicry theory states that frequency dependent selection should favour geographic convergence of harmful species onto a shared colour pattern. As such, mimetic patterns are commonly circumscribed into discrete mimicry complexes each containing a predominant phenotype. Outside a few examples in butterflies, the location of transition zones between mimicry complexes and the factors driving them has rarely been examined. To infer the patterns and processes of Müllerian mimicry, we integrate large-scale data on the geographic distribution of colour patterns of all social bumble bees across the contiguous United States and use these to quantify colour pattern mimicry using an innovative machine learning approach based on computer vision and image recognition. Our data suggests that bumble bees exhibit a manifold of similar, but imperfect colour patterns, that continuously transition across the United States, supporting the idea that mimicry is not discrete. We propose that bumble bees are mimicking a perceptual colour pattern average that is evolutionarily transient. We examine three comimicking polymorphic species, Bombus flavifrons, B. melanopygus, and B. bifarius, where active selection is driving colour pattern frequencies and determine that their colour pattern transition zones differ in location and breadth within a broad region of poor mimicry. Furthermore, we explore factors driving these differences such as mimicry selection dynamics and climate.
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Descriptive studies of natural history have always been a source of knowledge on which experimental work and scientific progress rely. Poison frogs are a well-studied group of small Neotropical frogs with diverse parental behaviors, distinct calls, and bright colors that warn predators about their toxicity; and a showcase of advances in fundamental biology through natural history observations. The dyeing poison frog, Dendrobates tinctorius, is emblematic of the Guianas region, widespread in the pet-trade, and increasingly popular in research. This species shows several unusual behaviors, such as the lack of advertisement calls and the aggregation around tree-fall gaps, which remain poorly described and understood. Here, we summarize our observations from a natural population of D. tinctorius in French Guiana collected over various field trips between 2009 and 2017; our aim is to provide groundwork for future fundamental and applied research spanning parental care, animal dispersal, disease spread, habitat use in relation to color patterns, and intra specific communication, to name a few. We report sex differences in habitat use and the striking invasion of tree-fall gaps; describe their courtship and aggressive behaviors; document egg development and tadpole transport; and discuss how the knowledge generated by this study could set the grounds for further research on the behavior, ecology, and conservation of this species.
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Variation in aposematic signals was once predicted to be rare, yet in recent years it has become increasingly well documented. Despite increases in the frequency with which polytypism and polymorphism have been suggested to occur, population-wide variance is rarely quantified. We comprehensively sampled a subpopulation of the poison frog Oophaga sylvatica, a species which is polytypic across its distribution and also shows considerable within-population polymorphism. On one hand, color pattern polymorphism could be the result of multifarious selection acting to balance different signaling functions and leading to the evolution of discrete sub-morphs which occupy different fitness peaks. Alternatively, variance could simply be due to relaxed selection, where variation would be predicted to be continuous. We used visual modeling of conspecific and heterospecific observers to quantify the extent of within population phenotypic variation and assess whether this variation produced distinct signals. We found that, despite considerable color pattern variation, variance could not be partitioned into distinct groups, but rather all viewers would be likely to perceive variation as continuous. Similarly, we found no evidence that frog color pattern contrast was either enhanced or diminished in the frogs’ chosen microhabitats compared to alternative patches in which conspecifics were observed. Within population phenotypic variance therefore does not seem to be indicative of strong selection toward multiple signaling strategies, but rather pattern divergence has likely arisen due to weak purifying selection, or neutral processes, on a signal that is highly salient to both conspecifics and predators.
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I observed a Rufous Motmot (Baryphthengus martii) feeding a black-and-green poison dart frog (Dendrobates auratus) to another motomot in the Caribbean Slope lowland rainforest of northeastern Costa Rica. Neither individual appeared to suffer any ill effects from what was probably courtship feeding. Small vertebrates are typical prey for the larger species of motmots. Blue-crowned Motmots (momotus momota) have been observed consuming several species of poison dart frogs raised in captivity but captive reared frogs either do not contain, or have reduced levels of, the toxins that native frogs produce. Relatively little is known about the effects of poison dart frog toxins on predators. Presumably, the digestive system of the Rufous Motmot is capable of neutralizing the potentially toxic effects of such prey.
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Animals can avoid predation by masquerading as objects that are not food to their predators. Alder moth Acronicta alni larvae go through an impressive ontogenetic change from masquerade to highly conspicuous appearance: early larval stages resemble bird droppings but in the last instar the larval coloration changes into striking yellow-and-black stripes. We hypothesized that such a change may be driven by differential predation favoring dissimilar anti-predator strategies in different life stages. We show with a series of laboratory assays that larvae are distasteful to birds regardless of their developmental stage, suggesting that ontogenetic color change is not driven by the differential chemical defense. Birds showed higher variance in hesitation toward conspicuous prey; some individuals hesitated long time before attacking whereas all birds attacked instantly masqueraded prey. We also found that the activity level of the larvae increased with age, which fits to the fact that larvae need to move from foliage to pupation sites. In the field by using artificial larvae resembling the two life-history stages we found predation risk to vary during the season: In early summer larger yellow-and-black larvae were attacked most, whereas later in the summer small 'bird-dropping-larvae' suffered the highest predation. We conclude that the ontogenetic switch from masquerading to aposematism is adaptive most likely because actively moving prey cannot mimic immotile objects and thus, aposematism during the active and vulnerable period when larvae are searching for pupation sites becomes beneficial.
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Aposematic signal variation is a paradox: predators are better at learning and retaining the association between conspicuousness and unprofitability when signal variation is low. Movement patterns and variable colour patterns are linked in non-aposematic species: striped patterns generate illusions of altered speed and direction when moving linearly, affecting predators’ tracking ability; blotched patterns benefit instead from unpredictable pauses and random movement. We tested whether the extensive colour-pattern variation in an aposematic frog is linked to movement and found that individuals moving directionally and faster have more elongated patterns than individuals moving randomly and slowly. This may help explain the paradox of polymorphic aposematism: variable warning signals may reduce protection, but predator defence might still be effective if specific behaviours are tuned to specific signals. The interacting effects of behavioural and morphological traits may be a key to the evolution of warning signals.
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Whether hybridization can be a mechanism that drives phenotypic diversity is a widely debated topic in evolutionary biology. In poison frogs (Dendrobatidae), assortative mating has been invoked to explain how new color morphs persist despite the expected homogenizing effects of natural selection. Here, we tested the complementary hypothesis that new morphs arise through hybridization between different color morphs. Specifically, we (1) reconstructed the phylogenetic relationships among the studied populations of a dart-poison frog to provide an evolutionary framework, (2) tested whether microsatellite allele frequencies of one putative hybrid population of the polymorphic frog O. histrionica are intermediate between O. histrionica and O. lehmanni, and (3) conducted mate-choice experiments to test whether putatively intermediate females prefer homotypic males over males from the other two populations. Our findings are compatible with a hybrid origin for the new morph and emphasize the possibility of hybridization as a mechanism generating variation in polymorphic species. Moreover, because coloration in poison frogs is aposematic and should be heavily constrained, our findings suggest that hybridization can produce phenotypic novelty even in systems where phenotypes are subject to strong stabilizing selection.
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1.Polymorphism in warning coloration is puzzling because positive frequency-dependent selection by predators is expected to promote monomorphic warning signals in defended prey. 2.We studied predation on the warning-coloured wood tiger moth (Parasemia plantaginis) by using artificial prey resembling white and yellow male colour morphs in five separate populations with different naturally occurring morph frequencies. 3.We tested whether predation favours one of the colour morphs over the other and whether that is influenced either by local, natural colour morph frequencies or predator community composition. 4.We found that yellow specimens were attacked less than white ones regardless of the local frequency of the morphs indicating frequency-independent selection, but predation did depend on predator community composition: yellows suffered less attacks when Paridae were abundant, whereas whites suffered less attacks when Prunellidae were abundant. 5.Our results suggest that spatial heterogeneity in predator community composition can generate a geographic mosaic of selection facilitating the evolution of polymorphic warning signals. This is the first time this mechanism gains experimental support. Altogether, this study sheds light on the evolution of adaptive coloration in heterogeneous environments. This article is protected by copyright. All rights reserved.
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Warning signals of aposematic organisms often include patterns that contrast with background coloration, though controversy exists over their importance. Many den-drobatids have contrasting colors, but no work has established whether these are anti-predator components of the warning signal. We used 840 clay frog models to test whether a black spotted pattern on the red dorsum of the poison frog Oophaga pumilio (= Dendrobates pumilio) from Costa Rica enhances the aposematic signal. Model type, patterned or not patterned, did not predict predation. However, we did find evidence that background (i.e., contrast between an aposematic organism and its environment) influenced a predator's attack decision because models on white paper (higher con-trast) were attacked significantly less than models on leaf litter (lower contrast). Our results indicate that the pattern of Costa Rican O. pumilio does not influence predation. Our results also support the hypothesis that novel backgrounds evoke a neophobic reaction and can affect predation rates.
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Because variation in warning signals slows down the predator education process, aposematic theory predicts that animal warning signals should be monomorphic. Yet, warning color polytypisms are not uncommon in aposematic species. In cases where warning signal variants are separated geographically, adaptation to local predators could explain this variation. However, this cannot explain the persistence of sympatric polymorphisms in aposematic taxa. The strawberry poison frog (Oophaga pumilio) exhibits both allopatric and sympatric warning color variation in and around the Bocas del Toro archipelago of Panama. One explanation that has been proposed for the rapid diversification of O. pumilio coloration in this archipelago is low predation; if island populations have few predators, stabilizing selection would be relaxed opening the door for diversification via selection or genetic drift. Using a combination of mark-recapture and clay model studies, we tested for differences in survival and predation among sympatric red and yellow color morphs of O. pumilio from Bastimentos Island. We found no evidence for differential survival or predation in this population, despite the fact that one morph (red) is more common and widely distributed than the other (yellow). Even in an area of the island where the yellow morph is not found, predator attack rates were similar among morphs. Visual modeling suggests that yellow and red morphs are distinguishable and conspicuous against a variety of backgrounds and by viewers with different visual systems. Our results suggest that general avoidance by predators of red and yellow, both of which are typical warning colors used throughout the animal kingdom, may be contributing to the apparent stability of this polymorphism.
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The persistence of novel aposematic forms, and thereby the evolution of aposematic polymorphism, remain intriguing. Novel and rare forms could be disproportionally attacked by predators that already learned to avoid a pre-existing and more common aposematic form. Alternatively, novel forms could be less frequently attacked if predators are reluctant to attack unknown potential prey (neophobia) or if previous learning allows them to generalise and recognise the novel form as toxic. We used colour variation in polymorphic poison frogs (Oophaga histrionica complex) to test whether predators familiar with one aposematic form do generalise their avoidance behaviour to other aposematic forms. To strengthen our inference, we combined a field test of attack rates to local and non-local models with a lab experiment of generalisation capabilities by newly born chicks. Field predators attacked a significantly lower proportion of 529 aposematic compared to 150 cryptic models. Predators co-occurring with the local aposematic form of O. histrionica equally avoided non-local forms, especially in areas where the species was abundant. Forty-two lab chicks learned to discriminate between an aposematic and a cryptic image, but failed to generalise to other aposematic images, even though we tried with six combinations of aposematic forms. To better mimic the situation in the field, we further tested whether chicks trained with a set of four simultaneous aposematic images would generalise better. They failed to learn the discrimination task. Our data contrast with previous field studies on other poison frogs, and support a role for generalisation, and arguably not neophobia, in predator avoidance of novel aposematic forms.
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Despite the predicted purifying role of stabilising selection against variation in warning signals, many aposematic species exhibit high variation in their colour patterns. The maintenance of such variation is not well understood, but it has been suggested to be the result of an interaction between sexual and natural selection. This interaction could also facilitate the evolution of sexual dichromatism. Here we analyse in detail the colour patterns of the poison frog Dendrobates tinctorius and evaluate the possible correlates of the variability in aposematic signals in a natural population. Against the theoretical pre- dictions of aposematism, we found that there is enormous intra-populational variation in colour patterns and that these also differ between the sexes: males have a yellower dorsum and bluer limbs than females. We discuss the possible roles of natural and sexual selection in the maintenance of this sexual dimorphism in coloration and argue that parental care could work synergistically with aposematism to select for yellower males.
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