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Genome size varies greatly across the tree of life and transposable elements are an important contributor to this variation. Among vertebrates, amphibians display the greatest variation in genome size, making them ideal models to explore the causes and consequences of genome size variation. However, high-quality genome assemblies for amphibians have, until recently, been rare. Here, we generate a high-quality genome assembly for the dyeing poison frog, Dendrobates tinctorius. We compare this assembly to publicly available frog genomes and find evidence for both large-scale conserved synteny and widespread rearrangements between frog lineages. Comparing conserved orthologs annotated in these genomes revealed a strong correlation between genome size and gene size. To explore the cause of gene-size variation, we quantified the location of transposable elements relative to gene features and find that the accumulation of transposable elements in introns has played an important role in the evolution of gene size in D. tinctorius, while estimates of insertion times suggest that many insertion events are recent and species-specific. Finally, we carry out population-scale mobile-element sequencing and show that the diversity and abundance of transposable elements in poison frog genomes can complicate genotyping from repetitive element sequence anchors. Our results show that transposable elements have clearly played an important role in the evolution of large genome size in D. tinctorius. Future studies are needed to fully understand the dynamics of transposable element evolution and to optimize primer or bait design for cost-effective population-level genotyping in species with large, repetitive genomes.
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Anuros , Elementos Transponibles de ADN , Evolución Molecular , Tamaño del Genoma , Genoma , Animales , Anuros/genética , Ranas VenenosasRESUMEN
Despite the great diversity of parental care types found in amphibians, studies linking them to post-copulatory sexually selected traits are scarce, presumably due to a lack of data. Valencia-Aguilar et al. used fieldwork and museum collections to show that paternal care appears to trade-off with testes size in glass frogs.
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Testículo , Animales , Testículo/anatomía & histología , Masculino , Conducta Paterna , Tamaño de los Órganos , Anuros/anatomía & histología , Anuros/fisiologíaRESUMEN
For animals that synthesise their chemical compounds de novo, resources, particularly proteins, can influence investment in chemical defences and nitrogen-based wing colouration such as melanin. Competing for the same resources often leads to trade-offs in resource allocation. We manipulated protein availability in the larval diet of the wood tiger moth, Arctia plantaginis, to test how early life resource availability influences relevant life history traits, melanin production and chemical defences. We expected higher dietary protein to result in more effective chemical defences in adult moths and a higher amount of melanin in the wings. According to the resource allocation hypothesis, we also expected individuals with less melanin to have more resources to allocate to chemical defences. We found that protein-deprived moths had a slower larval development, and their chemical defences were less unpalatable for bird predators, but the expression of melanin in their wings did not differ from that of moths raised on a high-protein diet. The amount of melanin in the wings, however, unexpectedly correlated positively with chemical defences. Our findings demonstrate that the resources available in early life have an important role in the efficacy of chemical defences, but melanin-based warning colours are less sensitive to resource variability than other fitness-related traits.
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Mariposas Nocturnas , Humanos , Animales , Melaninas/metabolismo , Larva/metabolismo , Dieta/veterinaria , Asignación de RecursosRESUMEN
Artisanal and small-scale gold mining (ASGM) has become a major threat for Neotropical forests. This technique for obtaining gold is a substantial driver of small-scale deforestation and the largest contributor of Hg emissions to both the atmosphere and freshwater systems globally. Previous studies have demonstrated the impacts of Hg accumulation on various aquatic ecosystems and organisms. However, its consequences in other, more discrete systems such as phytotelmata (water-holding plant structures), and the organisms therein, have so far gone unnoticed. Here, we show high concentrations of Hg (mean ± SD: 1.43 ± 2.19 ppm) in phytotelmata and other small pools, the aquatic microenvironments used by the Neotropical poison frog Dendrobates tinctorius as tadpole-rearing sites. In 17 % of the cases, we detected Hg concentrations above the severe effect level (SEL = 2 ppm) for freshwater sediments. Hg concentrations varied depending on pool characteristics and tended to increase in proximity to known ASGM sites. We did not find an effect of Hg concentration on the number of D. tinctorius tadpoles in a given pool. Tadpoles were found in pools with concentrations of up to 8.68 ppm, suggesting that D. tinctorius fathers do not avoid pools with high Hg levels for tadpole deposition. While further research is needed to determine the potential effects of Hg on tadpole development, we found an intriguing tendency for tadpoles in later developmental stages to have lower body condition when occurring in pools with higher Hg concentrations. Our findings provide evidence of relevant Hg concentrations in the terrestrial water systems used by phytotelm-breeding anurans, and highlight the need of further field and experimental studies investigating the implications of Hg contamination for tadpole development and behaviour and the overall conservation of Amazonian biodiversity.
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Mercurio , Ranas Venenosas , Venenos , Contaminantes Químicos del Agua , Animales , Mercurio/análisis , Larva , Ecosistema , Contaminantes Químicos del Agua/toxicidad , Contaminantes Químicos del Agua/análisis , Anuros , Oro , Agua , Monitoreo del AmbienteRESUMEN
Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.
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Ecología , Conducta Predatoria , Animales , FenotipoRESUMEN
Deimatic displays, where sudden changes in prey appearance elicit aversive predator reactions, have been suggested to occur in many taxa. These (often only putative) displays frequently involve different components that may also serve antipredator functions via other mechanisms (e.g., mimicry, warning signalling, body inflation). The Colombian four-eyed frog, Pleurodema brachyops, has been suggested to gain protection against predation through putative deimatic displays where they inflate and elevate the posterior part of their body revealing eye-like colour markings. We exposed stationary artificial frogs to wild predators to test whether the two components (eyespot/colour markings, defensive posture) of their putative deimatic display, and their combination, provide protection from predation without the sudden change in appearance. We did not detect any obvious additive effect of defensive posture and eyespots/colour markings on predation risk, but found a marginally significant trend for model frogs in the resting posture to be less attacked when displaying eyespots/colour markings than when they were not, suggesting that the presence of colour markings/eyespots may provide some protection on its own. Additionally, we found that models in a resting posture were overall more frequently attacked on the head than models in a defensive posture, indicating that a defensive posture alone could help redirect predator attacks to non-vital parts of the body. The trends found in our study suggest that the different components of P. brachyops' coloration may serve different functions during a deimatic display, but further research is needed to elucidate the role of each component when accompanied by sudden prey movement.
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Mariposas Diurnas , Postura , Animales , Colombia , Conducta PredatoriaRESUMEN
Turbidity challenges the visual performance of aquatic animals. Here, we use the natural diversity of ephemeral rearing sites occupied by tadpoles of two poison frog species to explore the relationship between environments with limited visibility and individual response to perceived risk. To compare how species with diverse natural histories respond to risk after developing in a range of photic environments, we sampled wild tadpoles of (1) Dendrobates tinctorius, a rearing-site generalist with facultatively cannibalistic tadpoles and (2) Oophaga pumilio, a small-pool specialist dependent on maternal food-provisioning. Using experimental arenas, we measured tadpole activity and space use first on a black and white background, and then on either black or white backgrounds where tadpoles were exposed to potentially predatory visual stimuli. The effects of rearing environment on D. tinctorius tadpoles were clear: tadpoles from darker pools were less active than tadpoles from brighter pools and did not respond to the visual stimuli, whereas tadpoles from brighter pools swam more when paired with conspecifics versus predatory insect larvae, suggesting that tadpoles can visually discriminate between predators. For O. pumilio, tadpoles were more active on experimental backgrounds that more closely matched the luminosity of their rearing sites, but their responses to the two visual stimuli did not differ. Larval specialisation associated with species-specific microhabitats may underlie the observed responses to visual stimuli. Our findings demonstrate that light availability in wild larval rearing conditions influences risk perception in novel contexts, and provides insight into how visually guided animals may respond to sudden environmental disturbances.
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Anuros , Natación , Animales , Larva/fisiología , Anuros/fisiología , Especificidad de la Especie , Conducta Predatoria/fisiologíaRESUMEN
Many chemically-defended/aposematic species rely on diet for sequestering the toxins with which they defend themselves. This dietary acquisition can lead to variable chemical defenses across space, as the community composition of chemical sources is likely to vary across the range of (an aposematic) species. We characterized the alkaloid content of two populations of the Dyeing Poison Frog (Dendrobates tinctorius) in northeastern French Guiana. Additionally, we conducted unpalatability experiments with naive predators, Blue Tits (Cyanistes caeruleus), using whole-skin secretion cocktails to assess how a model predator would respond to the defense of individuals from each population. While there was some overlap between the two D. tinctorius populations in terms of alkaloid content, our analysis revealed that these two populations are markedly distinct in terms of overall alkaloid profiles. Predator responses to skin secretions differed between the populations. We identified 15 candidate alkaloids (including three previously undescribed) in seven classes that are correlated with predator response in one frog population. We describe alkaloid profile differences between populations for D. tinctorius and provide a novel method for assessing unpalatability of skin secretions and identifying which toxins may contribute to the predator response. In one population, our results suggest 15 alkaloids that are implicated in predator aversive response. This method is the first step in identifying the causal link between alkaloids and behavioral responses of predators, and thus makes sense of how varying alkaloid combinations are capable of eliciting consistent behavioral responses, and eventually driving evolutionary change in aposematic characters (or characteristics).
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Alcaloides , Venenos , Pájaros Cantores , Toxinas Biológicas , Humanos , Animales , Venenos/toxicidad , Anuros/fisiología , Conducta Predatoria/fisiologíaRESUMEN
Chemical defences often vary within and between populations both in quantity and quality, which is puzzling if prey survival is dependent on the strength of the defence. We investigated the within- and between-population variability in chemical defence of the wood tiger moth (Arctia plantaginis). The major components of its defences, SBMP (2-sec-butyl-3-methoxypyrazine) and IBMP (2-isobutyl-3-methoxypyrazine), are volatiles that deter bird attacks. We hypothesized that (1) variation in the chemical defences of male wood tiger moths reflects the local predation pressure; (2) observed differences in quantity and quality of defence among populations have a genetic basis; and (3) increasing concentrations of SBMP and IBMP will elicit greater aversive reactions in predators, with the two pyrazines having an additive effect on predators' avoidance. We found that (1) the chemical defence of wild moths partly reflects local predator selection: high predation pressure populations (Scotland and Georgia) had stronger chemical defences, but not lower variance, than the low-predation populations (Estonia and Finland). (2) Based on the common garden results, both genetic and environmental components seem to influence the strength of chemical defence in moth populations; and (3) IBMP alone did not provide protection against bird predators but worked against bird attacks only when combined with SBMP, and while SBMP was more effective at higher concentrations, IBMP was not. Altogether this suggests that, when it comes to pyrazine concentration, more is not always better, highlighting the importance of testing the efficacy of chemical defence and its components with relevant predators, as extrapolating from chemical data may be less than straightforward.
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Mariposas Nocturnas , Animales , Masculino , Mariposas Nocturnas/genética , Aves , Pirazinas , Conducta Predatoria , ColorRESUMEN
Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders-Anura, Caudata, and Gymnophiona-there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.
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Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.
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Anuros , Conducta Animal , Animales , Femenino , Masculino , Andrógenos , Anuros/fisiología , Factores Sexuales , Conducta Animal/fisiologíaRESUMEN
In juveniles extreme intraspecies aggression can seem counter-intuitive, as it might endanger their developmental goal of surviving until reproductive stage. Ultimately, aggression can be vital for survival, although the factors (e.g., genetic or environmental) leading to the expression and intensity of this behavior vary across taxa. Attacking (and sometimes killing) related individuals may reduce inclusive fitness; as a solution to this problem, some species exhibit kin discrimination and preferentially attack unrelated individuals. Here, we used both experimental and modeling approaches to consider how physical traits (e.g., size in relation to opponent) and genetic relatedness mediate aggression in dyads of cannibalistic Dendrobates tinctorius tadpoles. We paired full-sibling, half-sibling, and non-sibling tadpoles of different sizes together in an arena and recorded their aggression and activity. We found that the interaction between relative size and relatedness predicts aggressive behavior: large individuals in non-sibling dyads are significantly more aggressive than large individuals in sibling dyads. Unexpectedly, although siblings tended to attack less overall, in size-mismatched pairs they attacked faster than in non-sibling treatments. Using a theoretical model to complement these empirical findings, we propose that larval aggression reflects a balance between relatedness and size where individuals trade-off their own fitness with that of their relatives. Lay SummaryBefore you eat someone, you have to attack them first. Here, we investigated the factors that shape aggression in the cannibalistic tadpoles of the dyeing poison frog. We find that aggression depends on both size and relatedness: when set in pairs, large tadpoles are half as aggressive towards their smaller siblings than to nonsibs. It looks like belonging to the same family provides some protection against aggression, though no one is ever truly safe.
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Many organisms have evolved adaptations to increase the odds of survival of their offspring. Parental care has evolved several times in animals including ectotherms. In amphibians, ~ 10% of species exhibit parental care. Among these, poison frogs (Dendrobatidae) are well-known for their extensive care, which includes egg guarding, larval transport, and specialized tadpole provisioning with trophic eggs. At least one third of dendrobatids displaying aposematism by exhibiting warning coloration that informs potential predators about the presence of defensive skin toxins. Aposematism has a central role in poison frog diversification, including diet specialization, and visual and acoustic communication; and it is thought to have impacted their reproductive biology as well. We tested the latter association using multivariate phylogenetic methods at the family level. Our results show complex relationships between aposematism and certain aspects of the reproductive biology in dendrobatids. In particular, aposematic species tend to use more specialized tadpole-deposition sites, such as phytotelmata, and ferry fewer tadpoles than non-aposematic species. We propose that aposematism may have facilitated the diversification of microhabitat use in dendrobatids in the context of reproduction. Furthermore, the use of resource-limited tadpole-deposition environments may have evolved in tandem with an optimal reproductive strategy characterized by few offspring, biparental care, and female provisioning of food in the form of unfertilized eggs. We also found that in phytotelm-breeders, the rate of transition from cryptic to aposematic phenotype is 17 to 19 times higher than vice versa. Therefore, we infer that the aposematism in dendrobatids might serve as an umbrella trait for the evolution and maintenance of their complex offspring-caring activities.
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Anuros/fisiología , Conducta Animal , Evolución Biológica , Mimetismo Biológico/fisiología , Conducta Materna , Animales , Femenino , Larva , Masculino , Filogenia , ReproducciónRESUMEN
Many species of Neotropical frogs have evolved to deposit their tadpoles in small water bodies inside plant structures called phytotelmata. These pools are small enough to exclude large predators but have limited nutrients and high desiccation risk. Here, we explore phytotelm use by three common Neotropical species: Osteocephalus oophagus, an arboreal frog that periodically feeds eggs to its tadpoles; Dendrobates tinctorius, a tadpole-transporting poison frog with cannibalistic tadpoles; and Allobates femoralis, a terrestrial tadpole-transporting poison frog with omnivorous tadpoles. We found that D. tinctorius occupies pools across the chemical and vertical gradient, whereas A. femoralis and O. oophagus appear to have narrower deposition options that are restricted primarily by pool height, water capacity, alkalinity, and salinity. Dendrobates tinctorius tadpoles are particularly flexible and can survive in a wide range of chemical, physical, and biological conditions, whereas O. oophagus seems to prefer small, clear pools and A. femoralis occupies medium-sized pools with abundant leaf litter and low salinity. Together, these results show the possible niche partitioning of phytotelmata among frogs and provide insight into stressors and resilience of phytotelm breeders.
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Animals are often difficult to distinguish at an individual level, and being able to identify individuals can be crucial in ecological or behavioral studies. In response to this challenge, biologists have developed a range of marking (tattoos, brands, toe-clips) and tagging (banding, collars, PIT, VIA, VIE) methods to identify individuals and cohorts. Animals with complex life cycles are notoriously hard to mark because of the distortion or loss of the tag across metamorphosis. In amphibians, few studies have attempted larval tagging and none have been conducted on a tropical species. Here, we present the first successful account of VIE tagging in early larval stages (Gosner stage 25) of the dyeing poison frog (Dendrobates tinctorius) coupled with a novel anesthetic (2-PHE) application for tadpoles that does not require buffering. Mean weight of individuals at time of tagging was 0.12 g, which is the smallest and developmentally youngest anuran larvae tagged to date. We report 81% tag detection over the first month of development, as well as the persistence of tags across metamorphosis in this species. Cumulative tag retention vs tag observation differed by approximately 15% across larval development demonstrating that "lost" tags can be found later in development. Tagging had no effect on tadpole growth rate or survival. Successful application of VIE tags on D. tinctorius tadpoles introduces a new method that can be applied to better understand early life development and dispersal in various tropical species.
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Warning signals are predicted to develop signal monomorphism via positive frequency-dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large-scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth, Arctia plantaginis, differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.
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Mariposas Nocturnas , Animales , Aves , Color , Finlandia , Conducta Predatoria , EscociaRESUMEN
Despite rising interest among scientists for over two centuries, parental care behavior has not been as thoroughly studied in amphibians as it has in other taxa. The first reports of amphibian parental care date from the early 18th century, when Maria Sibylla Merian went on a field expedition in Suriname and reported frog metamorphs emerging from their mother's dorsal skin. Reports of this and other parental behaviors in amphibians remained descriptive for decades, often as side notes during expeditions with another purpose. However, since the 1980s, experimental approaches have proliferated, providing detailed knowledge about the adaptive value of observed behaviors. Today, we recognize more than 30 types of parental care in amphibians, but most studies focus on just a few families and have favored anurans over urodeles and caecilians. Here, we provide a synthesis of the last three centuries of parental care research in the three orders comprising the amphibians. We draw attention to the progress from the very first descriptions to the most recent experimental studies, and highlight the importance of natural history observations as a source of new hypotheses and necessary context to interpret experimental findings. We encourage amphibian parental care researchers to diversify their study systems to allow for a more comprehensive perspective of the behaviors that amphibians exhibit. Finally, we uncover knowledge gaps and suggest new avenues of research using a variety of disciplines and approaches that will allow us to better understand the function and evolution of parental care behaviors in this diverse group of animals.
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Chloe Fouilloux and colleagues introduce animal cannibalism.
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Canibalismo , Animales , HumanosRESUMEN
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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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.