ArticleLiterature Review

Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns

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Abstract

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.

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... In the absence of advertisement calls, the use of tactile stimuli and both static (such as dorsal color patterns) and dynamic visual signals most likely plays a predominant role in D. tinctorius communication. Dorsal color patterns might mediate mate choice (Rojas, 2017), given that individuals follow each other for a considerable amount of time while searching for a suitable place for oviposition. Males have been found to have a higher proportion of yellow in their dorsal area than females in our study population (Rojas & Endler, 2013). ...
... This has been suggested to be particularly beneficial during tadpole transport (Rojas & Endler, 2013), a task that requires long displacements and prolonged exposure (Pašukonis, Loretto & Rojas, 2019), especially when climbing trees. Male coloration might thus indicate parental male quality and be subject to sexual selection (Rojas, 2017). The variable coloration patterns on these frogs' front, forelimbs, and flanks, could also have the potential to be used as signals, as a lot of the time the frogs are either facing or next to each other during courtship (Rojas, 2012). ...
... Aggressive behavior and territoriality in D. tinctorius might be context-dependent and related to population density, variation in food abundance and other resources, such as structures for shelter or oviposition. In the absence of vocalizations, D. tinctorius may be using visual signals to get information about the fighting abilities of their opponents, as it has been reported for male O. pumilio (Crothers, Gering & Cummings, 2011;Crothers & Cummings, 2015), and settle their conflicts before escalating to physical combats (Rojas, 2017). Social behavior in D. tinctorius is a promising avenue of research, which could provide insights into the evolution of visual communication and factors influencing anuran aggressive and territorial behavior in the absence of acoustic communication. ...
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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.
... This phenomenon occurs in many invertebrates and vertebrates, but in most cases its drivers are not well understood. Colour in animals has several functions, such as camouflage, signaling for reproductive partners or predators and contribution to metabolism, i.e., protecting them against radiation (Davis and Grayson, 2008;Toledo and Haddad, 2009;Rojas, 2017;Lambert et al., 2017). At the intraspecific level, colour change has been linked to adaptations to physiological, behavioural, and environmental requirements (Grant et al., 2007;Wilson, Heinsohn and Endler, 2007;Cortesi et al., 2016;Bulbert et al., 2018). ...
... At the intraspecific level, colour change has been linked to adaptations to physiological, behavioural, and environmental requirements (Grant et al., 2007;Wilson, Heinsohn and Endler, 2007;Cortesi et al., 2016;Bulbert et al., 2018). Amphibians have a wide variety of colour patterns and signals whose evolutionary and ecological significance has been poorly studied (Hoffman and Blouin, 2000;Toledo and Haddad, 2009;Rojas, 2017). ...
... factors can also relate to the variable measured, such as age, that in turn has been associated with size, sexual maturation, and other diverse traits on anuran species (i.e., Iturra-Cid, Ortiz and Ibarguengoytía, 2010; Marangoni et al., 2012;Cajade, Marangoni and Gangenova, 2013;Huang et al., 2013;Arantes et al., 2015;Quiroga, Sanabria and Marangoni, 2015). It is also important to acknowledge that despite making only a few inferences about reproduc-tion and predator-prey relationships, which are the most common associations of colour function in anurans (Toledo and Haddad, 2009;Rojas, 2017), other approaches such as UV protection, thermoregulation and diet can also be significant (Rudh and Qvarnström, 2013;Umbers et al., 2016). Lastly, colour can show plasticity in response to environmental variables and some interactions (such as climate, predation and food availability) in some anuran species (Touchon et al., 2010;Brenes-Soto, Dierenfeld and Janssens, 2017;Franco-Belussi, Provete and De Oliveira, 2017;Pintanel et al., 2019). ...
Article
Ontogenetic colour change (OCC) is defined as the progressive and non-reversible process of changes in colouration of organisms associated with their development. Among the many vertebrate groups, amphibians are particularly impressive for their strikingly wide variety of colours, colour patterns, and signals, whose evolutionary and ecological significance have been poorly studied. Elachistocleis comprises 18 species currently separated into two main groups based on their ventral colour pattern: one immaculate and the other with specks and/or colour patches. Elachistocleis haroi is a small-sized species within the immaculate venter group, distributed in the Yungas and Dry Chaco ecoregions from which little information is known. In a comprehensive sampling of post-metamorphic individuals of E. haroi at different stages of development we identified a significant variation in ventral colour pattern, which could denote a progressive filling of yellow colour according to an ontogenetic pattern. To test this hypothesis, we analysed 39 post-metamorphic individuals of E. haroi at different stages of development with imaging procedures. We found that yellow spots and their intensity are significantly related to snout-vent length, as major expansion of colour on the sides, gular region and male chest, as almost no development on the belly. We briefly discuss our findings in relation to sexual display and predation avoidance. To our knowledge, this is the first analysis of post-metamorphic OCC in ventral colouration in the genus Elachistocleis .
... Once variation has arisen in allopatry, it may then be reinforced through mechanisms related to local predation pressure, assortative mating or intraspecific agonistic interactions, or a combination of several factors, which can further drive divergence between genetically and physically isolated populations (Gray and McKinnon, 2007;Briolat et al., 2019). Variation can, however, also arise in sympatric populations without physical barriers to gene flow (Rojas, 2017;Briolat et al., 2019). The mechanisms underlying the evolution and persistence of this variance are, however, less well understood, and in many cases it is still unclear whether such variation has evolved for an adaptive function. ...
... Some of the most salient examples of phenotypic variation are found in the Neotropical poison frogs (Dendrobatidae), which exhibit notable examples of both discrete and continuous variation in color and pattern, found both in sympatry (polymorphism) and allopatry (polytypism) (Summers et al., 2003;Maan and Cummings, 2012;Rojas, 2017). Color patterns have evolved both for defensive and communicative functions, and in many cases under the influence of multiple selection pressures (Summers et al., 1999;Saporito et al., 2007;Maan and Cummings, 2008Wollenberg et al., 2008;Tazzyman and Iwasa, 2010;Crothers et al., 2011;Cummings and Crothers, 2013;Rudh, 2013;Crothers and Cummings, 2015;Dreher et al., 2015). ...
... Moreover, in O. pumilio certain phenotypes and behaviors are correlated with microhabitats which enhance signal efficacy (Pröhl and Ostrowski, 2011;Willink et al., 2014), although they do not appear to be behaviorally manipulating saliency on fine scales (Dugas et al., 2020). In another polymorphic and polytypic poison frog species, Dendrobates tinctorius, sympatric color variation can also correlate with specialization in specific microhabitats, or behavioral syndromes that optimize signal saliency within their chosen microhabitats (Rojas et al., 2014a,b;Rojas, 2017). ...
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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.
... Amphibians are an ideal model system to examine the evolutionary relationships between parental care, sexual dimorphism, and body colorations and patterns. Amphibians are a speciesrich group (Wake and Koo 2018) that are colorful (Rojas 2017), dichromatic (Bell et al. 2017), and show some of the most diverse forms of caregiving behaviors (Wells 2007). Nearly 30 types of parental care behaviors have been documented in approximately 20% of the extant 8200 species of amphibians (Crump 2015;Furness and Capellini 2019;Vági et al. 2019;Schulte et al. 2020) and yet, our understanding of the evolution of parental care in amphibians is still lagging compared to other vertebrates (Stahlschmidt 2011). ...
... Camouflage may enable adult anurans to offset predation risk and may explain the prevalence of green, brown, and grey dorsal colors that effectively match natural substrates (Wells 2007;Rojas 2017). Crypticity of these dorsal colors is further aided by patterns such as mottling, stripes, bands, or spots (Choi and Jang 2004;Nilsson Skold et al. 2013;Kang et al. 2016) and even metachrosis (Duellman and Trueb 1994). ...
... For example, striped patterns are particularly effective in motion dazzle, whereas barred patterns are effective in flicker fusion during movement (Stevens and Merilaita 2011). Several anuran families use warning coloration or are aposematic (i.e., with chemical defense) to advertise unpalatability to predators (Wells 2007;Rojas 2017), and only recently has the role of body coloration in decreasing predation risk been observed among one group of anurans (e.g., poison-dart frogs; Carvajal-Castro et al. 2021). Although there is an increasing amount of evidence for how lifehistory traits shape body colors and patterns in taxonomic groups such as birds (Dale et al. 2015;Ekanayake et al. 2015;McQueen et al. 2019), none, to the best of our knowledge, examine if parental care is associated with sexual dichromatism and specific dorsal colors and patterns in anurans. ...
Article
Parental care is widespread and has fitness benefits. But caregiving parents incur costs including higher predation, and this may lead to selection for body colours or patterns that help mitigate the risks of caring. The evolution of colouration, including sexual dichromatism, however, can be driven by other factors, such as sexual selection. Therefore, examining the associations between parental care and colour patterns may provide key insights into evolutionary patterns and selection pressures for parental care. Our comparative analysis of 988 anuran species reveals that dichromatic species are less likely to provide parental care, irrespective of the caregiving sex, and are more likely to breed in aquatic habitats. We then examined whether dorsal colours and patterns that enhance crypticity or function as aposematic signals are associated with the caregiving sex and, the modality of care (transport or stationary). Only caregiving males are more likely to have dorsal Stripes, but none of the colours (Green‐Brown, Red, Yellow, Blue‐Black) and other patterns (Plain, Bands, Spots, Mottled‐Patches) were associated with caregiving females or the modality of care. Overall, sexual dichromatism, breeding ecology and parental care are associated, but the evolution of caregiving behaviour does not appear to influence the myriad colours and patterns characteristic of anurans globally. This article is protected by copyright. All rights reserved
... Sexual dichromatism, where males and females differ in coloration, has provided essential evidence for understanding sexual selection (Andersson 1994) and has been predominantly studied in birds (Dunn et al. 2015), fishes (Kodric-Brown 1998), and butterflies (Allen et al. 2011). In amphibians, it has been described in Bufonidae, Hylidae, Hyperoliidae, Ranidae, and Dendrobatoidea (Grant et al. 2006;Bell and Zamudio 2012;Bell et al. 2017;Rojas 2017;Portik et al. 2019), but unfortunately, the functional implications are mostly unknown. ...
... Several species of neotropical poison frogs from the superfamily Dendrobatoidea, which includes the sister clades Aromobatidae and Dendrobatidae, are well-known for the presence of aposematic coloration and recognizable coloration patterns (Silverstone 1975a(Silverstone , 1976Myers and Daly 1976;Grant et al. 2006Grant et al. , 2017Brown et al. 2011;Rojas 2017). Yet, cryptic coloration is also a common feature of different genera in both families (Grant et al. 2006(Grant et al. , 2017Rojas 2017). ...
... Several species of neotropical poison frogs from the superfamily Dendrobatoidea, which includes the sister clades Aromobatidae and Dendrobatidae, are well-known for the presence of aposematic coloration and recognizable coloration patterns (Silverstone 1975a(Silverstone , 1976Myers and Daly 1976;Grant et al. 2006Grant et al. , 2017Brown et al. 2011;Rojas 2017). Yet, cryptic coloration is also a common feature of different genera in both families (Grant et al. 2006(Grant et al. , 2017Rojas 2017). Sexual dichromatism in Dendrobatoidea is relatively common in cryptically colored species within Aromobatidae, but is absent or inconspicuous in most aposematic species (Bell et al. 2017;Grant et al. 2017;Greener et al. 2020). ...
Article
Sexual dichromatism has provided important information for understanding sexual selection , but its link to reproductive success has received little attention. Poison frogs and their relatives within the superfamily Dendrobatoidea present striking color variation. Despite this variability, evidence of sexual dichromatism in the over 330 species described is limited to the gular region of some cryptically colored species. Colostethus imbricolus is a cryptically colored dendrobatid with distinct orange and yellow spots at the axillar, ingui-nal and femoral regions. Here we show that these spots stand clearly out from the environment during behavioral displays and that they present marked sexual differences in their conspicuousness, with females having more conspicuous spots. Unlike most species of Dendrobatoidea that provide parental care in the form of male tadpole transport, we found that in C. imbricolus, females performed this behavior. By correlating color measurements and behavioral observations, we show that females with a higher number of transported tadpoles are also the most conspicuous. Our findings show a significant association between sexual dichromatism of the spots and female parental care while opening exciting perspectives for the occurrence of both traits. In addition, our results provide significant insights to address the function of dual-color patterns (i.e., cryptic from distance-apose-matic from nearby) in amphibians.
... detritivorous fungi; Sherratt, Wilkinson & Bain, 2005) (e.g. poison frogs that derive their defences from arthopods; Rojas, 2017). Finally, many endogenous defences originally evolved for another purposefor example, prey capture, such as the venom in snakes and centipedes (Greene & McDiarmid, 2005). ...
... Yet a positive correlation between warning colors and visible, risky behaviours are not evident in all warning-signalling taxa or at all life stages. In dendrobatid frogs the association between warning signals and habitat is unclear (Rojas, 2017). Coral snakes and their mimics are primarily fossorial, generally being hidden from sight in the leaf litter or in decaying logs (Campbell, Lamar & Brodie, 2004). ...
Article
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Warning signals are a striking example of natural selection present in almost every ecological community – from Nordic meadows to tropical rainforests, defended prey species and their mimics ward off potential predators before they attack. Yet despite the wide distribution of warning signals, they are relatively scarce as a proportion of the total prey available, and more so in some biomes than others. Classically, warning signals are thought to be governed by positive density-dependent selection, i.e. they succeed better when they are more common. Therefore, after surmounting this initial barrier to their evolution, it is puzzling that they remain uncommon on the scale of the community. Here, we explore factors likely to determine the prevalence of warning signals in prey assemblages. These factors include the nature of prey defences and any constraints upon them, the behavioural interactions of predators with different prey defences, the numerical responses of predators governed by movement and reproduction, the diversity and abundance of undefended alternative prey and Batesian mimics in the community, and variability in other ecological circumstances. We also discuss the macroevolution of warning signals. Our review finds that we have a basic understanding of how many species in some taxonomic groups have warning signals, but very little information on the interrelationships among population abundances across prey communities, the diversity of signal phenotypes, and prey defences. We also have detailed knowledge of how a few generalist predator species forage in artificial laboratory environments, but we know much less about how predators forage in complex natural communities with variable prey defences. We describe how empirical work to address each of these knowledge gaps can test specific hypotheses for why warning signals exhibit their particular patterns of distribution. This will help us to understand how behavioural interactions shape ecological communities.
... However, given the taxonomic prevalence, and the complexity of the unken reflex behavior, its antipredator function must still be better assessed. Results from Bordignon et al. (2018) and the present study corroborate the hypothesis that the unken reflex is a deimatic strategy (Umbers, Lehtonen & Mappes, 2015;Rojas, 2017;Bordignon et al., 2018). Therefore, not only the final posture or the exhibition of bright colors, but also the movement inherent to the unken reflex may be necessary to repel predators. ...
... Therefore, not only the final posture or the exhibition of bright colors, but also the movement inherent to the unken reflex may be necessary to repel predators. In this case, the species avoids detection as a primary strategy, and only uses the unken reflex to frighten their predators and avoid subjugation (Umbers et al., 2015;Rojas, 2017). With regard to the startle reflexes of predators (Umbers & Mappes, 2016;Caro & Allen, 2017), the unken reflex could potentially evolve as a deimatic strategy even in the scenario of a weak unpalatability signal, as discussed for M. cambaraensis. ...
Article
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Crypsis and aposematism are important forms of antipredatory strategies. Through cryptic coloration, animals reduce their detectability by matching the coloration of backgrounds, while through aposematic coloration, prey species signal to potential predators their unprofitability by conspicuous coloration. The efficacy of aposematism depends on a predator’s ability to identify and avoid unprofitable prey. Among amphibians, both strategies are well known for many species. Most species of red‐bellied toads, Melanophryniscus spp., present conspicuous coloration with a likely aposematic function, both dorsally and ventrally, and display the behavior known as the unken reflex. However, there are a few species, like M. cambaraensis, that only present ventral conspicuous coloration. The dorsal coloration of this species is dull green, which is usually associated with camouflage. Although this species is diurnal and toxic, the exposition of red ventral coloration does not seem to serve as an aposematic signal. Here, we evaluated experimentally if the green dorsal color of M. cambaraensis functions as warning coloration for visually oriented natural predators. We conducted field predation experiments using clay models, representing M. cambaraensis (green models) and a generalized cryptic frog (brown models), to compare attack rates between treatments. The avian attacks were concentrated mainly on the anterior end, suggesting models were perceived as prey. However, attack rates were similar on green and brown frog models. Our results suggest that the green dorsal color of the species does not act as an aposematic signal, but functions as a cryptic color. Although crypsis in poisonous species remains a complex topic, under certain circumstances, the selection pressures imposed by predators may favor a cryptic coloration instead of a conspicuous coloration, even for diurnal species. First published on line: 11 October 2019
... Previous studies have shown variation in toxicity among populations of dendrobatid poison frogs (e.g. Maan and Cummings 2012;Wang 2011), which has been attributed to the heterogeneity of arthropod communities from which alkaloids are sequestered (Maan and Cummings 2012;Rojas 2017;Wang 2011), and to different predation pressures (Wang 2011;Willink et al. 2014). In contrast, we did not find significant differences in toxicity, assessed through an irritant assay, among studied localities for P. vittatus. ...
... Among the dendrobatid frog family, the genus Phyllobates has been considered aposematic (Santos et al. 2003;Rojas 2017), meaning that the conspicuous coloration of the individuals is a warning signal of unpalatability or toxicity to potential predators (Ruxton et al. 2004;Skelhorn et al. 2016). 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). ...
Article
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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.
... During the first deployment, black models had a higher probability of bird attack than both striped and yellow models. Our data invoke two nonmutually exclusive hypotheses to explain the mechanism by which corroboree frog coloration influences predator behavior: (a) that the Southern Corroboree Frog color pattern may hinder predator detection by disruptive camouflage or (b) that birds may detect, but preferentially avoid the striped pattern on first encounter because innately they associate the coloration with unprofitability (i.e., aposematism) ( Lindström et al., 1999;Mappes et al., 2005;Rojas, 2017). Future experiments should test whether the stripes have a deterring function at close distance, but a concealing effect at long distance (Tullberg, Merilaita, & Wiklund, 2005). ...
... Contrary to expectations for a black-and-yellow striped frog, our data suggest that corroboree frog coloration makes them difficult to detect. Perhaps they are camouflaged and toxic-or perhaps they are camouflaged at a distance, but the yellow and black coloration renders them aposematic when viewed up close (Rojas, 2017). Such hypotheses are for future work in sensory ecology. ...
Article
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After decades of near‐complete extirpation, the yellow‐and‐black‐striped Southern Corroboree Frog (Pseudophryne corroboree) is being reintroduced into field enclosures that exclude all but avian predators. The frog's long absence means avian attack risk to reintroduced individuals is unknown, so we asked: does corroboree frog coloration make them vulnerable to predators? First, using painted clay frog models and humans as proxy predators, we found that, surprisingly, striped models were as difficult to detect as control black models, and were far less detectable than yellow models. Second, to quantify attack probabilities, we deployed 2,304 models twice in the species' former range. Of our recovered models, 18% of the striped models were attacked by birds, suggesting they are a significant threat. In our second deployment, we saw a significant reduction in attacks on all model colors with only 10% of striped models attacked. If predators generalize their avoidance learning to real corroboree frogs, strategically timed model deployment near release sites may enhance the probability of survival of reintroduced frogs. Our study suggests that model deployment could be an effective low‐cost technique to increase the survival of reintroduced prey species, including, but not limited to, those potentially conspicuous to their natural enemies.
... We also provide a test that supports our hypothesis that throat colour provides a signal of female quality. Reviews of the occurrence of conspicuous colouration in frogs [2,3] emphasise two general cases. First, aposematic (warning) signals to other species indicate that these frogs are well protected by toxins. ...
... The adaptive significance of female sexual dichromatism in Mannophryne seems clear: it is associated with territorial defence. Territorial behaviour in dendrobatids is common, but mainly involves males [2]. Long-term defence of a territory by female frogs, as occurs in Mannophryne (extrapolating from the species where it has been demonstrated, such as M. trinitatis and M. collaris), is very rare. ...
Article
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Recent reviews on sexual dichromatism in frogs included Mannophryne trinitatis as the only example they could find of dynamic dichromatism (males turn black when calling) within the family Aromobatidae and found no example of ontogenetic dichromatism in this group. We demonstrate ontogenetic dichromatism in M. trinitatis by rearing post-metamorphic froglets to near maturity: the throats of all individuals started as grey coloured; at around seven weeks, the throat became pale yellow in some, and more strongly yellow as development proceeded; the throats of adults are grey in males and variably bright yellow in females, backed by a dark collar. We demonstrated the degree of throat colour variability by analysing a large sample of females. The red: green (R:G) ratio ranged from ~1.1 to 1.4, reflecting variation from yellow to yellow/orange, and there was also variation in the tone and width of the dark collar, and in the extent to which the yellow colouration occurred posterior to the collar. Female M. trinitatis are known to be territorial in behaviour. We show a positive relationship between throat colour (R:G ratio) and escape performance, as a proxy for quality. Our field observations on Tobago’s M. olmonae showed variability in female throat colour and confirmed that males in this species also turn black when calling. Our literature review of the 20 Mannophryne species so far named showed that all females have yellow throats with dark collars, and that male colour change to black when calling has been reported in eight species; in the remaining 12 species, descriptions of males calling are usually lacking so far. We predict that both dynamic and ontogenetic sexual dichromatism are universal in this genus and provide discussion of the ecological role of dichromatism in this genus of predominantly diurnal, non-toxic frogs, with strong paternal care of offspring.
... The evolution of chromatic specialization and toxicity is a recurrent pattern in anurans. Tetrodotoxin or analogues have been identified in conjunction with aposematic coloration in several anuran families: Brachycephalidae, Bufonidae, Mycrohylidae, Myobatrachidae, Dendrobatidae and Rhacophoridae (Hanifin, 2010;Rojas, 2017). Our data show that conspicuous coloration has evolved multiple times in the evolutionary history of Brachycephalus, generally in species with larger body sizes. ...
... The biological function of colours and colour patterns has been studied in predator-prey interactions, intraspecific communication, sexual selection and habitat use (Hödl & Amézquita, 2001;Bell & Zamudio, 2012;Rojas, 2017). Literature records suggest that aposematic species of Brachycephalus suffer less predation than other syntopic anurans, and when they are attacked it is usually by visually oriented predators, such as birds (Carvalho, 1941;Toledo & Haddad, 2007), confirming that the bright colour can provide visual warning related to toxicity. ...
Article
Evolutionary changes towards a miniaturized body plan may directly affect other important phenotypic traits related to the physiology, behaviour and ecology of organisms. The frog genus Brachycephalus is an outstanding example of a radiation of miniaturized species endemic to the Brazilian Atlantic Forest. We inferred ancestral states and historical changes in body size, body colour and hyperossification to test hypotheses about diversification and selective environmental mechanisms leading to the evolution of these specialized traits. The ancestral distribution was associated with high-elevation regions in the northern Serra do Mar mountain range, and diversification in the genus was coincident with important geological and climatic events during the history of the Atlantic Forest. The dynamic historical changes provided an opportunity for multiple lowland lineages and for speciation via dispersal and vicariance in multiple invasions of the highlands. The ancestral Brachycephalus was reconstructed as miniaturized and dull coloured, without hyperossification in the skin, skull or postcranial skeleton. A parallel evolution of phenotypic traits has occurred in northern and southern Atlantic Forest lineages, beginning in the Miocene. Shifts in body size are not related to elevation range or latitude. However, we found a significant correlation between the evolution of hyperossification and aposematism with increasing body size.
... Within a species, color is important during inter-and intra-sexual selection, as it can signal reproductive status, age, or individual quality (e.g., birds: Part and Qvarnström 1997, Keyser and Hill 1999, Badyaev and Duckworth 2003, Hanssen et al. 2006mammals: Setchell et al. 2006, Bergman et al. 2009amphibians: Brenes-Soto et al. 2017, Zamora-Camacho andComas 2018;fish: Hippel 1999;reptiles: Cuadrado 2000, Weiss 2006; insects: Kemp 2007, Willink et al. 2019reviewed in Cuthill et al. 2017). Among species, color can honestly advertise unpalatability levels to predators (e.g., Boyden 1976, Schlee 1986, Maan and Cummings 2012 or, alternatively, deceive predators through background matching, masquerade or Batesian mimicry (reviewed in Stoddard 2012, Rojas 2017, Merilaita et al. 2017). ...
... Color and pattern polymorphisms have been described in over 200 species of frogs (Hoffman and Boulin 2000), with over 100 of showing sexual dichromatism (Bell and Zamudio 2012). Still, the processes that influence the evolution and maintenance of color variation in amphibians remain poorly understood (reviewed in Hoffman and Blouin 2000, Bell and Zamudio 2012, Rojas 2017, Merilaita et al. 2017). Our study takes new steps towards understanding these patterns, emphasizing the need for research that simultaneously addresses eco-physiological mechanisms as well as multiple hypotheses within the gamut of selective pressures influencing the evolution of coloration. ...
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Animal coloration is a multifaceted trait with many ecological roles and related to a variety of developmental and physiological processes. Consequently, coloration is often subject to a variety of selective pressures, leading to the evolutionary maintenance of variation. In this study, we investigated hypotheses related to the maintenance of dorsal color variation in wood frogs (Rana sylvatica). First, we tested for multimodality, and whether color correlates with body size or condition or varies by sex or age‐class. We combined behavioral trials with visual modeling to test for sex recognition. We also considered visual models for predators and tested for an interaction between discriminability indexes (JND) of color channel (chromatic vs. achromatic) and predator type (birds vs. snakes), as well as for a within individual trade‐off between the JND of chromatic and achromatic coloration. Finally, we tested for disruptive viability selection on color using predation trials, and for antagonistic directional selection between viability selection and reproductive investment of females. We found that wood frogs present continuous color variation that does not correlate with body size or condition, but that changes with age. Wood frogs present subtle sexual dichromatism, but we found no evidence for a role of color in sex recognition. Instead, we discuss the possibility that sex differences might, at least in part, have a demographic explanation. Predator visual models indicated that wood frogs cannot solely rely on dorsal coloration for camouflage. Moreover, different predators might present selective pressures in different color channels, while individuals’ achromatic and chromatic coloration trade‐off in JND. Therefore, different selective pressures caused by different predators might interact with ontogenetic changes and developmental/physiological trade‐offs to maintain color variation. We found no relationship between color and survival or reproductive investment, suggesting further work is required to fully understand selection on color. Our results highlight the importance of understanding evolutionary trade‐offs and developmental/physiological constraints in combination with one another, and suggest the potential for an interaction between these proximate and ultimate mechanisms in the evolutionary maintenance of variation. These results likely extend beyond color expression in amphibians, and exemplify a more general process for such evolutionary outcomes.
... Anurans display a striking diversity of colouration which is often closely tied with avoiding predators, the most widespread function of which is camouflage (Rojas, 2017). Cryptic body colour prevents detection or recognition of anurans by their predators (Cooper et al., 2008). ...
... However, this does not necessarily mean that these frogs are easily found by their predators. For example, the frogs might be masquerading as a dead leaf; masquerading is an antipredator strategy, where an animal resembles an object that is uninteresting to their predators (Rojas, 2017). Factors other than predator avoidance could also affect their diurnal resting sites and colouration. ...
... The color patterns of poison frogs (Dendrobatidae) are incredibly diverse and often display highly contrasting colors and patterning. Visual signals can vary tremendously both between and within species but, despite sampling dozens of populations, reflection of wavelengths outside of the spectrum visible to humans has not been described to date (Hoogmoed & Avila-Pires, 2012;Roberts et al., 2007;Rojas, 2017;Siddiqi et al., 2004;Twomey et al., 2016;Wang & Shaffer, 2008;Yeager et al., 2012). Intraspecific variation may be discrete or continuous and is found both in sympatry and in allopatry (Rojas, 2017). ...
... Visual signals can vary tremendously both between and within species but, despite sampling dozens of populations, reflection of wavelengths outside of the spectrum visible to humans has not been described to date (Hoogmoed & Avila-Pires, 2012;Roberts et al., 2007;Rojas, 2017;Siddiqi et al., 2004;Twomey et al., 2016;Wang & Shaffer, 2008;Yeager et al., 2012). Intraspecific variation may be discrete or continuous and is found both in sympatry and in allopatry (Rojas, 2017). The function and evolution of this diversity have been the focus of much research, and poison frog color has been variously linked to aposematism, camouflage, and sexual signaling (Crothers & Cummings, 2015;Hegna et al., 2013;Maan & Cummings, 2008;Richards-Zawacki et al., 2012;Saporito et al., 2007;Summers et al., 1999;Tazzyman & Iwasa, 2010;Willink et al., 2013;Yang et al., 2019). ...
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Aposematic and sexual signals are often characterized by bright, highly contrasting colors. Many species can see colors beyond the human visible spectrum, and ultraviolet (UV) reflection has been found to play an important role in communication and sexual selection. However, the role of UV in aposematic signals is poorly explored. Poison frogs frequently produce high‐contrast signals that have been linked to both aposematism and intraspecific communication. Yet despite considerable efforts studying interspecific and intraspecific diversity in color, poison frogs are not known to perceive UV, and UV reflection of the integument has not been described. We report UV‐reflective spots in a population of Oophaga sylvatica and quantify the effect of UV on visual contrast with models of avian vision. We found that the frogs are highly contrasting, but UV had a minimal effect on signal saliency. These data highlight the importance of considering UV reflectance within aposematic signals, but that UV should not necessarily be regarded as an independent signal.
... This visual communication system is known as aposematism (Steven, 2013), a widespread phenomenon that independently evolved many times in different amphibians lineages (Wells, 2007). Aposematic colourations are usually associated with a variety of toxic compounds that are produced or sequestered and stored in specialised glandular skin glands (e.g., Wells, 2007;Rojas, 2017;Demori et al., 2019). Several species of aquatic and terrestrial salamanders exhibit a variety of combinations of red, orange yellow or white marks usually displayed on brown or black backgrounds. ...
... In salamanders, conspicuous colourations are typically assumed to act as aposematic warning anti-predatory signals (e.g., Wells, 2007;Lüddecke et al., 2018). In fact, several alkaloids (e.g., tetradoxins) and other toxic compounds are isolated from the skin of newts and salamanders, reinforcing the assumption that these contrasted colourations are associated with unpalatability (e.g., Yotsu-Yamashita et al., 2007, 2017Preissler et al., 2019). ...
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Aposematism is a visual communication system in which bright and contrasted coloured prey warn predators about their unprofitability. The Northern Spectacled Salamander Salamandrina perspicillata, a small terrestrial sal-amander endemic to Italy, displays a uniform dark dorsal colouration and a contrasted ventral side in which a bright red colour is displayed by coiling the tail over the body. In amphibians, this behaviour, known as "Unkenreflex", is usually considered to be aposematic. In this study, we used realistic plasticine replicas to test this aposematic hypothesis in the Northern Spectacled Salamander. Of the 199 clay models placed in a natural habitat, 165 (83%) were recovered and 39 (24%) showed some sign of predation. The head of the models was more attacked than expected by chance (P = 0.042), suggesting that potential predators were perceiving models as real prey. However, there were no differences in the proportion of dorsal (18/83 = 22%), and ventral (21/82 = 26%) models attacked by predators. Therefore, contrary to expectations our experiment did not support the aposematic hypothesis. However, predation experiments with clay models have limitations and our results should be considered as preliminary, deserving further research to better understand the Northern Spectacled salamander prey-predator system.
... Sexual selection has been suggested to play a crucial role in shaping amphibian coloration (reviewed in Rojas 2016). For example, in some populations of O. pumilio males are significantly more brightly colored than females (Solarte Island), and females prefer brighter males (In three populations) (Maan and Cummings 2009). ...
... However sexual selection may act on other sexually dimorphic traits in O. lehmanni such as the presence of white spots on their limbs. This frog exhibits an elaborate courtship in which males display foot flagging and arm waving, similar to other anurans who display colored parts in reproductive contexts (Hödl and Amezquita 2001;Rojas 2016). It would also be interesting to examine the toe-pad size, which is a sexually dimorphic trait in D. tinctorius (Rojas and Endler 2013). ...
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Territoriality and parental care are complex reproductive behaviors found in many taxa from insects to mammals. Parental care can be carried out by the female, the male, or both, depending on the species. Territoriality, in contrast, is predominantly displayed by males. Different selective pressures imposed on individuals from the sex performing territorial or parental care behaviors may also lead to sexual differentiation in other life-history traits. Due to their territorial behavior and their diversity of parental care behaviors, Neo-tropical poison frogs are an excellent study system to investigate whether behavioral traits can influence sexual differentiation in intrinsic or extrinsic traits of individuals. Here, we evaluate whether territorial and parental care behaviors mediate sexual differentiation in ecological (habitat use) and phenotypic (coloration, morphology) traits in the critically endangered Lehmann's poison frog (Oophaga lehmanni), a species in which males defend territories while females provide parental care. We found sex differences in habitat use and morphological traits, but not in coloration. Males use trunks and green leaves as perches more frequently and are found on higher substrates, than females. We found no sex differences in body size, but females have longer arms than males, which is probably associated with their parental duties (climbing trees to feed the tadpoles). Altogether, our results provide evidence that selection pressures act differently on male and female traits, and that territoriality and parental care may promote the evolution of sexual differentiation in dendrobatids. Long-term wildlife observations are essential to identify important life-history traits and to evaluate hypotheses about the behavioral ecology and conservation of this and other vertebrate species.
... En ranas y sapos (Amphibia: Anura) han evolucionado diversas modalidades sensoriales que permiten a los individuos comunicarse intra e interespecíficamente [1][2][3]. Sin embargo, es la emisión, percepción y decodificación de señales acústicas, el sistema de comunicación más frecuentemente utilizado en estos vertebrados [4,5;Figura 1]. Previos trabajos [5,6] han propuesto cuatro categorías de señales acústicas en anuros (i.e. ...
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Vocalizations are one of the most important communication modalities in amphibian biology, and advertisement call is the type of vocalization mostly emitted by anurans (frogs and toads). In the present study, we carried out a scientometric analysis of the advertisement call in species of anurans in Colombia to determine the state of knowledge of this science in the country. We recorded the number of call descriptions and its trend throughout more than 60 years; in addition, we identified how many species there are with the call described per taxonomic family, geographic units and threat status. According to our review, between 1958 and June 30 of 2021, at least 296 studies have been published that describe the advertisement call of 307 species (of 785 in the country); only 130 descriptions come from recordings to individuals in Colombian populations. Leptodactylidae and Hylidae are the families with the highest percentage of species whose call has been described (84.6% and 68.4%, respectively). On the contrary, Bufonidae (19.5%) and Craugastoridae (12.9%) exhibit a low percentage of described calls. The Central and Eastern cordilleras were the regions with the best knowledge of advertisement calls, while the least known were the Caribbean – interAndean valleys, Orinoquía, and Sierra Nevada de Santa Marta. In terms of the threat status, the species with the least concern (LC) were the ones that presented the highest number of species with the call described. Despite an increase in the most recent two decades, our findings still reveal notable gaps in knowledge of the advertisement calls in Colombian anurans, which constitutes an incentive to develop future research on this subject. Finally, based on this meta-analysis, we highlight some recommendations that we hope that we hope stimulate new studies in ecoacoustics, using anurans in Colombia as a study model.
... Nevertheless, phenotypic variation and polymorphism in aposematic organisms are widespread in nature (e.g. frogs: Rojas, 2017;Siddiqi et al., 2004;newts: Beukema et al., 2016;Mochida, 2011;butterflies: Merrill et al., 2015;moths: Brakefield and Liebert, 1985;bumblebees: Plowright and Owen, 1980;beetles: Bocek and Bocak, 2016;Brakefield, 1985;locusts: Nabours, 1929;myriapods: Marek and Bond, 2009;nudibranchs: Winters et al., 2017), which requires an evolutionary explanation. ...
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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. A geographic mosaic of selection by predators could explain the paradoxical maintenance of warning signal variation, but direct ecological evidence is scarce and focused on tropical systems. We monitored local avian predators and attacks on 4000 + moth models representing red, yellow or white warning colour morphs in a temperate moth system with natural variation in local morph frequencies. We found positive frequency‐dependent selection to be strongest in monomorphic populations and the direction and strength of selection to be significantly associated with local predator community composition and diversification, which can explain not only geographic variation (polytypism) but also local polymorphism when coupled with gene flow.
... Why Mantella have such large genomes is not yet known. The striking similarity in M. baroni and M. madagascariensis coloration and pattern as well as their toxicity are thought to be a case of Müllerian mimicry since the two species occur sympatrically and belong to two different clades Rojas, 2017;Schaefer et al., 2002;Vences, Chiari, Raharivololoniaina, & Meyer, 2004). Our finding raises the question on whether the long genome size found in these two species is related to their aposematic coloration pattern and the use of Müllerian mimicry as a defensive strategy or their capacity to eat and secrete alkaloids. ...
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Within the Malagasy endemic family of Mantellidae, the only completely sequenced mitochondrial genome (mitogenome) is that of Mantella madagascariensis. Yet, this genome has proven to be the largest among all vertebrates with 23 kbp in size, and shows a duplication of the tRNA methionine coding gene, a pseudogene of this same gene and a duplicated control region. In this study, we report the complete mitochondrial genome of Mantella baroni, the second mitogenome sequenced for the Mantellidae family. This genome sequence has been generated using next-generation sequencing technics performed on Illumina Hi-seq. The genome is 20,945 bp (21 kbp) in size with 13 protein-coding genes, 23 tRNA coding genes, 2 rRNA coding genes and 2 Control Regions (CR1 and CR2). This newly generated mitogenome shows duplication of the tRNA glycine coding gene (G1 and G2) and translocation of tRNA methionine coding gene M2 in the CR2. This gene organization is unique among anurans. Both M. baroni and M. madagascariensis mitogenomes are amongst the largest in vertebrates which might be related to their aposematism or their skin toxicity by alkaloid secretion. We also hypothesize that other Mantella species likely have large genomes, being not clear how the genome size and organization of mitochondria evolved in Malagasy frogs. Testing such a hypothesis require more mitogenome sequencing for Mantella and other representatives of the mantellid diversity. The mitogenome generated here will be useful for comparative genomic studies but also to answer the question on how mitogenomes evolved in the Mantellidae family.
... toxic alkaloids), such as those in Dendrobatidae (poison frogs), can promote amplexus diversification. Several lineages of poison frogs have evolved aposematic coloration (Santos et al., 2003;Rojas, 2017), which is associated with a high diversification in acoustic communication signals as an alleged indirect effect of a reduction in predation pressure (Santos et al., 2014); thus, aposematism could also allow an increase in the complexity of courtship behaviours, promoting matings where axillary amplexus is not necessary. Our results support such intuition, because ≥22 dendrobatid species exhibit cephalic amplexus, whereas 18 species exhibit no amplexus (Weygoldt, 1987;Castillo-Trenn & Coloma, 2008). ...
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The evolution and diversification of animal reproductive modes have been pivotal questions in behavioral ecology. Amphibians present the highest diversity of reproductive modes among vertebrates, involving various behavioral, physiological and morphological traits. One of such features is the amplexus, the clasp or embrace of males on females during reproduction, which is almost universal to anurans. Hypotheses about the origin amplexus are limited and have not been thoroughly tested, nor had they taken into account evolutionary relationships in most comparative studies. However, these considerations are crucial to understand the evolution of reproductive modes. Here, using an evolutionary framework, we reconstruct the ancestral state of amplexus in 686 anuran species; investigate whether the amplexus type is a conserved trait; and test whether sexual size dimorphism (SSD) could have influenced the amplexus type or male performance while clasping females. Overall, we found evidence of at least 35 evolutionary transitions in amplexus type across anurans. We also found that amplexus exhibits a high phylogenetic signal (it is conserved across Anura evolutionary history) and the amplexus type does not evolve in association with SSD. We discuss the implications of our findings on the diversity of amplexus types across anurans.
... For example, effective antipredator 276 chemical defenses (i.e., toxic alkaloids) such as those in Dendrobatidae (poison frogs) can 277 promote amplexus diversification. Several lineages of poison frogs have evolved aposematic 278 coloration ( Santos et al., 2003;Rojas, 2017), which is associated with a high diversification in cephalic amplexus, whereas 18 species exhibit no amplexus (Weygoldt, 1987;Castillo-Trenn 284 & Coloma, 2008). Moreover, most species of Dendrobatidae are prolonged breeders (Wells, 285 1977), mostly terrestrial, highly territorial and whose oviposition occurs in hidden places 286 under leaflitter and tree roots (Wells, 1978;Pröhl, 2005;Summers & Tumulty, 2014;Rojas & 287 Pašukonis, 2019). ...
... In Anura, previous studies have linked colour characteristics and chromatic diversity to sexual selection (Summers et al., 1997;Reynolds & Fitzpatrick, 2007;Maan & Cummings, 2008Hettyey et al., 2009;Rojas, 2016;Dreher et al., 2017). For example, empirical evidence shows that sexual dichromatism may act as a type of visual signal evolved to promote swift mate recognition and mate finding in dense aggregations (Sztatecsny et al., 2012;Rehberg-Besler et al., 2015). ...
Article
Ancestral character-state reconstruction is a powerful method in phylogenetics that can be applied to elucidate the evolutionary history of secondary sexual characters. Here, we surveyed the variation and reconstructed the ancestral states of secondary sexual characters (i.e. sexual dichromatism, vocal slits and nuptial pads) for the most species-rich genus of anurans (Pristimantis) using maximum parsimony, maximum-likelihood and Bayesian methods. This study demonstrates that at least five independent transformation series account for the occurrence of sexual dichromatism in Pristimantis: dorsum, throat, venter, groin and posterior surface of thighs. The ancestral reconstructions suggest that the most recent common ancestor of Pristimantis lacks sexual dichromatism on these five body areas. Likewise, the occurrence of vocal slits and the absence of nuptial pads were inferred as ancestral conditions. Morphological synapomorphies were identified for Yunganastes and two infrageneric units within Pristimantis (the Pristimantis devillei and Pristimantis unistrigatus species groups). Our results demonstrate that the evolutionary history of the secondary sexual characters in Pristimantis followed a rather complex pattern of multiple independent gains and losses for which this genus is a promising model to investigate the evolution of secondary sexual characters in the context of the complex interactions between natural and sexual selection.
... Many compelling examples of natural selection in the wild have come from studying colour-pattern variation across diverse empirical systems (e.g., Corl et al., 2010;Hoekstra et al., 2004;Lowry et al., 2012;Nachman et al., 2003;Pfeifer et al., 2018;Rosenblum et al., 2004;Streisfeld & Kohn, 2005;Supple et al., 2015;Twomey et al., 2015). In animals, colour and colour pattern can play important ecological roles, serving as, for example, a deterrent to predation (crypsis, aposematism), as a signal to conspecifics (mate choice, territoriality) or both (Cummings & Crothers, 2013;Rojas, 2016;Selz et al., 2016;Stevens & Merilaita, 2009). Accordingly, colour and colour pattern are often shaped by selection, and variation in colour traits can provide insight into the evolutionary dynamics that shape diversity. ...
Article
Investigating the spatial distribution of genetic and phenotypic variation can provide insights into the evolutionary processes that shape diversity in natural systems. We characterized patterns of genetic and phenotypic diversity to learn about drivers of color-pattern diversification in red-eyed treefrogs (Agalychnis callidryas) in Costa Rica. Along the Pacific coast, red-eyed treefrogs have conspicuous leg color patterning that transitions from orange in the north to purple in the south. We measured phenotypic variation of frogs, with increased sampling at sites where the orange-to-purple transition occurs. At the transition zone, we discovered the co-occurrence of multiple color-pattern morphs. To explore possible causes of this variation, we generated a SNP dataset to analyze population genetic structure, measure genetic diversity, and infer the processes that mediate genotype-phenotype dynamics. We investigated how patterns of genetic relatedness correspond with individual measures of color pattern along the coast, including testing for the role of hybridization in geographic regions where orange and purple phenotypic groups co-occur. We found no evidence that color-pattern polymorphism in the transition zone arose through recent hybridization. Instead, a strong pattern of genetic isolation by distance (IBD) indicates that color-pattern variation was either retained through other processes such as ancestral color polymorphisms or ancient secondary contact, or else it was generated by novel mutations. We found that phenotype changes along the Pacific coast more than would be expected based on genetic divergence and geographic distance alone. Combined, our results suggest the possibility of selective pressures acting on color pattern at a small geographic scale.
... A relationship between lower body condition and duller coloration was also observed. The implication of the differences observed could be negative survival or lower reproductive success if captive frogs were to be released to the wild (Rojas, 2016). The hue comparison results showed that the golden mantella frogs' skin coloration has been affected by captivity with a significant difference when compared to wild conspecifics. ...
Article
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Coloration is an important trait for social communication in amphibians, being used in intra- and intersexual signalling to express information about individual body condition and health state, amongst other things. The striking colour pattern exhibited by some anuran species are also used in “aposematic” signals to advertise unpalatability to predators. The aim of this study was to investigate how the captive environment affects the colour of golden mantella frogs by comparing captive reared frogs with wild conspecifics. A USB-2000 portable diode-array spectrometer and a xenon strobe light source were used to perform spectrophotometric measurements on captive and wild populations. Hue, chroma and brightness of skin colour were analysed as well as body condition using the scaled mass index. Analyses showed variation among populations, but significant differences were only found between captive and wild populations. Generalised linear mixed models were used to evaluate the effects of body condition on colour variation and showed that animals with lower body condition from one captive population had significantly different coloration than their wild counterparts. Importantly, one captive population was not greatly different in coloration from their wild counterparts – demonstrating that this problem is not inevitable in captivity. These results can have important implications for reintroduction programmes.
... Although both conspicuous colors and sexual dichromatism have evolved multiple times in amphibians (Bell and Zamudio 2012), we know surprisingly little about the benefits and costs for males expressing bright coloration (Zamora-Camacho and Comas 2019), and the function of color in female choice for nocturnal species. For instance, nocturnal amphibians still perceive and use color and color patterns as signals (Bell et al. 2017, Robertson and Greene 2017, Rojas 2017; thus, we could expect the information transmitted through male coloration signals to be similar to those already documented in fish, birds, and primates (Hill 1991, Grether et al. 1999, Waitt et al. 2003, Hubbard et al. 2010, including signaling of genetic and phenotypic quality and the potential for more attractive offspring (Huk and Winkel 2008). Yet, the costs of signal honesty in amphibians are less known. ...
Article
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Sexual selection can drive variation in conspicuous traits, providing signals to females about overall male health including their ability to fight parasites. Trait–parasite relationships have been extensively studied in fish and birds, but few records exist for amphibians. Here, we focused on a direct‐developing frog (Eleutherodactylus cooki) that exhibits variation in the extent of yellow coloration on the venter of males, a sexually selected trait that is correlated with reproductive success and parental care. We quantified the relationship between the color trait and the prevalence of two parasites, a tick (Carios undescribed sp.) and a fungal pathogen (Batrachochytrium dendrobatidis), across hosts, populations, and environmental contexts. We found that tick larvae were carried more frequently by males than females. Among males, ticks parasitized more those with a greater extent of yellow coloration. We did not detect any patterns associated with sex, habitat use, or male coloration with fungal infections. Co‐infections were low (5%) and predominantly occurred in males (71%). Our findings highlight the reproductive cost of tick parasitism for males and suggest that females may assess both the quality of parental care and overall health in areas of high tick exposure. Thus, yellow coloration in males of this nocturnal amphibian may have evolved as an honest signal of health and quality of parental care.
... Thus, it is possible that spatiotemporal variation in selection may have contributed to the successful establishment of the novel colour morphs (Rojas, 2017). Founder populations with distinct coloration patterns can become fixed by a combination of drift and positive frequency dependent selection driven by predators (Sherratt, 2006;Tazzyman & Iwasa, 2010). ...
Article
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Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, O. anchicayensis and the critically endangered O. lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early‐generation hybrids and thus, they likely did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they likely represent an independent lineage which has persisted through isolation and has only relatively recently re‐established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic color morphs, potentially via context‐dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.
... First, predation risk itself can vary over time due to changes in the composition of the predator species, their population density, or their foraging activity, which consequently, can alter the selection on prey color patterns for background matching (Bond, 2007;Caro, Sherratt, & Stevens, 2016;Endler, 1978). Second, seasonal changes in habitat structure and color (e.g., white snow in winter and green vegetation in summer) can also affect the selection of phenotypic characteristics for crypsis (Mills et al., 2013;Rojas, 2016;Steen, Erikstad, & Høidal, 1992;Tullberg, Gamberale-Stille, Bohlin, & Merilaita, 2008;Zimova, Mills, Lukacs, & Mitchell, 2014 Here, we quantified color patterns of a highly variable lizard species across space and seasons. Our study had three objectives: (a) to investigate the spatial variation in color patterns for background matching across a vegetation gradient; (b) to assess the potential signaling function of color variation by testing for correlations with age, sex, and quality; and (c) to determine if there is a trade-off between the need for crypsis and intraspecific signaling in color patterns across seasons along a vegetation gradient. ...
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--OPEN ACCESS-- Abstract In heterogeneous habitats, camouflage via background matching can be challenging because visual characteristics can vary dramatically across small spatial scales. Additionally, temporal variation in signaling functions of coloration can affect crypsis, especially when animals use coloration seasonally for intraspecific signaling (e.g., mate selection). We currently have a poor understanding of how wild prey optimize background matching within continuously heterogeneous habitats, and whether this is affected by requirements of intraspecific signaling across biological seasons. Here, we quantified color patterns of a wild population of shore skink (Oligosoma smithi), a variably colored lizard endemic to New Zealand, to (a) investigate whether background matching varies across a vegetation gradient; (b) assess potential signaling functions of color; and (c) to determine whether there is a trade‐off between requirements for crypsis and intraspecific signaling in coloration across seasons. Although all pattern types occurred throughout the vegetation gradient, we found evidence for background matching in skinks across the vegetation gradient, where dorsal brightness and pattern complexity corresponded with the proportion of vegetation cover. There was also a significant disparity between ventral color (saturation) of juveniles and adults, and also between sexes, suggestive of sex recognition. However, there was little indication that color was condition‐dependent in adults. Despite some evidence for a potential role in signaling, crypsis did not greatly differ across seasons. Our study suggests that selection favors a mix of generalist and specialist background matching strategies across continuously heterogeneous habitats.
... toxic alkaloids), such as those in Dendrobatidae (poison frogs), can promote amplexus diversification. Several lineages of poison frogs have evolved aposematic coloration (Santos et al., 2003;Rojas, 2017), which is associated with a high diversification in acoustic communication signals as an alleged indirect effect of a reduction in predation pressure (Santos et al., 2014); thus, aposematism could also allow an increase in the complexity of courtship behaviours, promoting matings where axillary amplexus is not necessary. Our results support such intuition, because ≥22 dendrobatid species exhibit cephalic amplexus, whereas 18 species exhibit no amplexus (Weygoldt, 1987;Castillo-Trenn & Coloma, 2008). ...
Article
The evolution and diversification of animal reproductive modes have been pivotal questions in behavioural ecology. Amphibians present the highest diversity of reproductive modes among vertebrates, involving various behavioural, physiological and morphological traits. One such feature is the amplexus, which is the clasp or embrace of males on females during reproduction and is found almost universally in anurans. Hypotheses about the origin of amplexus are limited and have not been tested thoroughly, nor have they taken into account evolutionary relationships in most comparative studies. However, these considerations are crucial to an understanding of the evolution of reproductive modes. Here, using an evolutionary framework, we reconstruct the ancestral state of amplexus in 685 anuran species. We investigate whether the type of amplexus has a strong phylogenetic signal and test whether sexual size dimorphism could have influenced amplexus type or male performance while clasping females. Overall, we found evidence of ≥34 evolutionary transitions in amplexus type across anurans. We found that amplexus type exhibits a high phylogenetic signal and that amplexus type does not evolve in association with sexual size dimorphism. We discuss the implications of our findings for the diversity of amplexus types across anurans.
... Even the most toxic prey, however, are preyed upon at least occasionally by predators. For example, poison frogs are consumed by birds, snakes, crabs and spiders (Rojas, 2017) and some toxic salamanders fall victim to snakes that have evolved immunity to their defences (Brodie, Ridenhour & Brodie, 2002). Thus, under some conditions, it could be beneficial even for aposematic prey to reduce detection through crypsis, so long as their warning signals can still be identified once detected (Wüster et al., 2004). ...
Article
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Antipredator adaptations in the form of animal coloration are common and often multifunctional. European vipers (genus Vipera) have a characteristic dorsal zigzag pattern, which has been shown to serve as a warning signal to potential predators. At the same time, it has been suggested to decrease detection risk, and to cause a motion dazzle or flicker–fusion effect during movement. We tested these hypotheses by asking whether (1) the zigzag pattern decreases detection risk and (2) the detection is dependent on the base coloration (grey or brown) or the snake's posture (coiled, basking form or S-shaped, active form). Additionally, (3) we measured the fleeing speed of adders, Vipera berus, and calculated the flicker rate of the zigzag pattern, to see whether it is fast enough to cause a flicker–fusion effect against predators. Our results show that the zigzag pattern reduced detectability regardless of base coloration or posture of the snake. The brown zigzag morph was detected less often than the grey zigzag morph. The fleeing speed of adders appeared to be fast enough to induce a flicker–fusion effect for mammalian predators. However, it is unlikely to be fast enough to induce the flicker–fusion effect for raptors. Our findings highlight that the colour pattern of animals can be multifunctional. The same colour pattern that can decrease detection by predators can also serve as a warning function once detected, and potentially hinder capture during an attack.
... Although it can be tempting to equate sexually dimorphic traits such as dichromatism with sexual selection, several alternative mechanisms may also contribute to female-biased dichromatism in hyperoliids. For instance, aposematism is a widespread anti-predator mechanism in frogs that is typically accompanied by the presence of skin toxins (reviewed in Toledo and Haddad 2009;Rojas 2017) such as alkaloids (Daly 1995). Sex-specific differences in chemical defense have been documented in some frogs (Saporito et al. 2010;Jeckel et al. 2015), but in several dichromatic hyperoliid species neither sex contained alkaloids in their skin . ...
... In nature, optical camouflage or concealment to the surroundings has been a key strategy employed by many species for both selfprotection and predation [1][2][3][4][5][6] much in the same way. Many butterflies or frogs display specific patterned wing/skin colors that can easily blend into the surrounding leaves and grassplot [7,8]. Chameleons and cephalopods even can adaptively alter their skin color via tuning light-skin interactions according to their surroundings [9,10]. ...
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Camouflage techniques are an integral part of the natural world. Despite having developed many technological approaches, creating a solution which can simultaneously modulate its visible and infrared appearance remains a great challenge and highly desired. We present a moisture assisted photo-engineered textile that visually blends objects into the surroundings both in the visible and infrared spectrum. In our solution, moisture content inside has been rendered sensitive to ambient temperature variations, allowing the textile to self-adaptively adjust its thermal emissivity in the wide range of 0.8 to 0.27 with the temperature varying from 25.8 oC to 67.4 oC. Its visible appearance can also be tuned using an interferometric structural color filter to deliver a broad range of colors. The moisture assisted photo-engineered textile features a low-cost, biocompatible, flexible, lightweight and convenient approach for visible and self-adaptive infrared dual camouflage.
... In this manner, people displaying solid fluorescence might be straightforward markers of high individual quality, since they can manage the related expenses. (Rojas, 2017) ...
... The Neotropical poison frogs (Dendrobatidae) have become a model system for understanding visual ecology due to their highly variable, and often very conspicuous, color patterns and their possession of alkaloid toxins (Summers and Clough 2001;Siddiqi et al. 2004;Roberts et al. 2007;Wang and Shaffer 2008;Hoogmoed and Avila-Pires 2012;Yeager et al. 2012;Twomey et al. 2016;Rojas 2017). One species, Oophaga pumilio, exhibits an extreme degree of color variation in the Bocas del Toro archipelago in Panama. ...
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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.
... Furthermore, the evolutionary processes leading to generalist or specialist camouflage can also play out 67 within species. This frequently results in phenotypic variation, which may be apparent as discrete morphs 68 or as continuous variation, and may be found within populations of sympatric individuals or in allopatry 69 (Rojas, 2017). Bond (2007) defined two categories of sympatric polymorphism: generalist polymorphism 70 and specialist polymorphism. ...
Article
Optimal camouflage can, in principle, be relatively easily achieved in simple, homogeneous, environments where backgrounds always have the same color, brightness, and patterning. Natural environments are, however, rarely homogenous and species often find themselves viewed against varied backgrounds where the task of concealment is more challenging. One result of variable backgrounds is the evolution of intraspecific phenotypic variation which may either be generalized, with multiple similarly cryptic patterns, or specialized, with each discrete color form maximizing concealment against a single component of the background. We investigated the role of phenotypic variation in a highly variable population of the Neotropical toad Rhinella margaritifera using visual modeling and a computer-based detection task. We found that phenotypic variation was not divided into discrete color morphs and all toads were well camouflaged against the forest floor. However, although the whole population may appear to consist of random samples from the background, the toads were a particularly close match to the leaf litter, suggesting that they masquerade as dead leaves, which are themselves variable. Furthermore, rather than each color form being equally effective against a single background, each toad was specialized towards its own particular local surroundings, as suggested by a specialist strategy. Taken together, these data highlight the importance of background matching to a nominally masquerading species, as well as how habitat heterogeneity at multiple spatial scales may affect the evolution of camouflage and phenotypic variation.
... La presencia de macroglándulas localizadas en regiones estratégicas del cuerpo, principalmente en la región post-orbital, está asociada a la producción de secreciones como mecanismo de defensa avanzado [44,45]. Estos distintivos parches glandulares, además de patrones de coloración llamativos (aposemáticos), sugieren la existencia de un mecanismo antidepredatorio por toxicidad [46,47]. Esta hipótesis está apoyada por observaciones de campo al momento de captura de individuos de P. andinodiabolus y P. erythros donde notamos la producción de un exudado de aspecto lechoso en ambas especies. ...
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We describe a new glandular terrestrial frog of the Pristimantis (Anura: Craugastoridae) genus. The new species inhabits the high montane forests of the Cañar province in southern Ecuador. It differs from other terrestrial frogs by having a striking dark gray and red dorsal coloration, dorsal skin with a corrugated texture, a small tubercle on the eyelid and heel, absence of vomerine odontophores, and large glandular patches on the supratympanic area, arms and limbs. Our molecular analyses show that the new species is in a clade with P. orcesi and P. erythros. Based on our results, we redefine the orcesi group and suggest that it contains only three species (P. orcesi, P. erythros, and the new species); the group is diagnosed mainly by exhibiting conspicuous dermal macroglands on the head, body and legs.
... Female preferences for males that invest more in sexual signals might also confer indirect genetic benefits through a classic good-genes pathway (Forsman & Hagman, 2006;Welch, Semlitsch, & Gerhardt, 1998). Acoustic and colour signals are costly to produce (in terms of energy expense and increased exposure to predators and parasites; Kemp, Herberstein, & Grether, 2012;Rojas, 2016), and can reflect male body condition, body size and/or age (Vasquez & Pfennig, 2007), all of which have been linked to genetic quality (Felton et al., 2006;Gerhardt & Huber, 2002;Parris, Velik-Lord, & North, 2009;Rausch, Sztatecsny, Jehle, Ringler, & H€ odl, 2014;Welch et al., 1998). ...
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The sublethal effects of infectious disease on reproductive behaviour and mating success are not well understood. Here, we investigated predictors of male mating success in one of Australia's most critically endangered vertebrates: the northern corroboree frog, Pseudophryne pengilleyi. Using a genomic approach to assign parentage, we explored whether infection with the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), a pathogen responsible for amphibian declines globally, influenced male calling behaviour and mating success. We also explored whether male mating success was predicted by phenotypic traits (age, body size, coloration, call characters) that potentially signal genetic quality, and the soil moisture (water potential) of male-constructed terrestrial nests, which may directly impact offspring survival. We found that Bd significantly influenced male advertisement; Bd-infected males produced calls with significantly higher pulse repetition rates than uninfected males. Older males had a higher probability of mating; however, variation in the number of eggs in a nest was most strongly explained by an interaction between male Bd infection status and call pulse repetition rate. We propose that these relationships may result from either pathogen-mediated changes to host behaviour or host-mediated changes to behaviour (e.g. terminal investment). Regardless of the mechanism, this is the first evidence that male mating success in an amphibian can be influenced by male Bd infection status, highlighting a novel mechanism through which this virulent pathogen can affect amphibian fitness. More broadly, these findings add to a growing body of evidence that pathogens can alter the reproductive biology of their hosts. From a conservation perspective, increased consideration of how sexual selection operates in altered environments has the potential to assist with the management of threatened amphibians worldwide.
... Sometimes, those colours are associated with aggressive behaviours (Galeano & Harms, 2016), and depending on the colour tone, it can have ecological and energetic implications for the individual (Hill, 1996). Furthermore, single or multimodal signalling can be used by other individuals to evaluate fitness and body condition, i.e., to evaluate the opponent's RHP (Ryan, 1991;Wells & Schwartz, 2007;Luna et al., 2010;Rojas, 2017). ...
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Anurans are one of the most diverse groups of animals, with single and multi-modal communication forms commonly used to settle disputes over territory and to attract females. Thus, I aimed to evaluate if male white-edged treefrogs tend to attack smaller individuals and which morphometric factor is related to it. Advertisement calls of this species were recorded and used in a four-choice experiment with the emission of artificially designed calls. I evaluated which speaker individuals approached and if morphometric variables could predict it. I observed that individuals approached significantly more often towards the high-pitched call than other treatments, and the frequency to do so was predicted by the extension of orange colour in their legs. These results indicate that smaller individuals are actively excluded from calling sites.
... Prior residency overwhelms coloration in determining contest outcomes in some species (e.g., tree lizard:Zucker & Murray, 1996; wall lizard: Sacchi et al., 2009; Italian ruin lizard:Titone et al., 2018), but was found to be secondary or negligible in comparison to coloration in others (e.g., redflanked bush robin:Morimoto et al., 2006; viviparous lizard: Martin et al., 2016). Perhaps because most frogs rely on acoustic signals for communication, there is comparatively less research on the effect of coloration on male-male competition for this group(Rojas, 2017). In O. pumilio, our study suggests that asymmetries that stem from prior experiences and residency status override the effects of color and body size in mediating male territoriality. ...
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in aggression level, suggesting a potential dominance hierarchy between these di- vergent phenotypes. In a contact zone between red and blue-color morphs, we first removed territorial males from their calling sites, and examined whether certain color morph(s) were better at establishing in these now-vacant territories. We then staged a territorial contest by simultaneously releasing the original and the new occupant to their point of capture. Surprisingly, we found no significant effect of color on ac- quiring territories or winning staged contests. However, the original occupants won against the new occupant in 84% of the staged contests, revealing a strong prior resi- dence effect. This suggests that asymmetries that stem from prior residency over- ride coloration in predicting contest outcomes of male–male territorial contests in wild O. pumilio. Thus, contradicting our hypothesis, male–male territorial competition alone seems unlikely to exert selection on coloration in this contact zone. K
... In nature, optical camouflage or concealment to the surroundings has been a key strategy employed by many species for both selfprotection and predation [1][2][3][4][5][6] much in the same way. Many butterflies or frogs display specific patterned wing/skin colors that can easily blend into the surrounding leaves and grassplot [7,8]. Chameleons and cephalopods even can adaptively alter their skin color via tuning light-skin interactions according to their surroundings [9,10]. ...
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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 locations, among which the frequencies of hindwing warning coloration of aposematic 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 strongest in monomorphic Scotland, and in contrast, lowest in polymorphic Finland, where different predators favour different male morphs. +FDS was also found in Georgia, where the predator community was the least diverse, whereas in the most diverse avian community in Estonia, hardly any models were attacked. Our results support the idea that spatial variation in predator and prey communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.
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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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Carotenoids play an import role as one of the most prevalent pigments in animals. Carotenoid-based coloration accounts for striking sexually and naturally selected colour adaptations. Several anurans (frogs and toads) change body coloration either slowly and permanently between life stages (ontogenetic colour change), or rapidly and temporarily within minutes or hours (dynamic colour change). We investigated ontogenetic colour change from orange to green morphs in the Wallace's flying frog, Rhacophorus nigropalmatus, and tested the influence of dietary carotenoids on colour change during postmetamorphic development. At the age of 9 months, while all individuals still possessed orange-red body coloration, a 20-week-long feeding experiment was performed by supplying the frogs with either no carotenoid supplements or dietary carotenoids once or four times per week. A high carotenoid diet resulted in a faster increase in green colour chroma as well as higher levels of green and carotenoid chroma of back coloration. Less or no carotenoid supplementation led to an increase in UV-blue chroma, contributing to a dull turquoise appearance often observed in captive-bred and captive-raised anurans. In addition, we showed for the first time that Wallace's flying frogs also perform dynamic colour changes. We tested dynamic changes triggered either by 2 min tactile handling or varying 1 h dark and light conditions. Our results demonstrate that a high carotenoid diet facilitates rapid and reversible change of body coloration in response to a tactile stressor, an adaptation absent in frogs receiving no carotenoids. Dynamic colour changes were likewise observed in response to changing light conditions presumably camouflaging individuals and providing protection from UV irradiation. The ontogenetic and dynamic pigmentation changes are discussed in relation to mechanism and as a likely strategy to avoid predation both at different life stages and in different environments.
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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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Conspicuous visual signals play an important role in animal communication, both within and between species. Bright, colourful signals allow animals to discriminate between individuals and can inform behavioural decisions and social interactions. In many instances, conspicuous colouration appears to have evolved through sexual selection via female mate choice or male–male competition. Male Neotropical yellow toads, Incilius luetkenii, display bright‐yellow colouration during their brief explosive mating events and then revert to a cryptic, female‐like, brown colour following amplexus and fertilization. Recent research has revealed that the yellow colouration of males may serve as a sex identification signal and that males remain yellow in the presence of both males and females but darken without conspecific stimulus. However, there is considerable variation in the brightness of yellow colouration in courting males, ranging from dull olive‐green to vibrant lemon‐yellow. The function of this variation remains unknown. In this study, we conducted two‐choice model presentation trials to test one mechanism of sexual selection that may drive this variation: intersexual selection. Specifically, we set out to determine whether females differentiate between males based on their colouration. We presented females with two hyper‐realistic robotic model toads, with one model painted to match a bright‐yellow male and the other a dull‐yellow male. Using several metrics of choice, we found that females did not show a preference for bright or dull colouration. Our research suggests that variation in the intensity of male breeding colouration is not driven by female choice in this species. Our study is consistent with the idea that there may be limited opportunity for female choice to influence male‐trait expression in explosive breeders. Future research will address whether intrasexual selection may influence colour variation in male yellow toads.
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Adaptive coloration in amphibians is widespread and aids in camouflage, communication, and thermoregulation. Understanding the environmental factors that contribute to color variation is important for predicting how changes in climate and habitat parameters may alter amphibian fitness. Studies on toad coloration have focused on genetic elements, dorsal spot patterns, and juveniles, but less is known about the relationship between adult toad coloration and environmental conditions. The goal of this study was to examine dorsal color variation in adult American Toads (Anaxyrus americanus) in Erie County, Pennsylvania, USA, to determine how environmental and morphological factors influence coloration. We conducted visual surveys to sample adult toads across a habitat gradient and recorded several potential predictor variables (i.e., site elevation, substrate type, snout–vent length, and body surface temperature). We calibrated photographs of each toad and quantified red (R), green (G), and blue (B) color values within seven dorsal body regions. We summarized RGB values for each dorsal body region using a principal component analysis and used model selection approaches to select between models containing different predictor variables. The most supported model to explain the variation in color of all dorsal body regions contained only site elevation. On average, the body regions of all toads from higher elevation sites were darker than those of toads from lower elevations, but the amount of variation in dorsal coloration accounted for by elevation was low. Our results suggest that the factors that drive variation in toad dorsal coloration are complex, but that this trait is potentially sensitive to environmental changes.
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Investigating the spatial distribution of genetic and phenotypic variation can provide insights into the evolutionary processes that shape diversity in natural systems. We characterized patterns of genetic and phenotypic diversity to learn about drivers of color-pattern diversification in red-eyed treefrogs ( Agalychnis callidryas ) in Costa Rica. Along the Pacific coast, red-eyed treefrogs have conspicuous leg color patterning that transitions from orange in the north to purple in the south. We measured phenotypic variation of frogs across Pacific sites, with increased sampling at sites where the orange-to-purple transition occurs. At the transition zone, we discovered the co-occurrence of multiple color-pattern morphs. To explore possible causes of this variation, we generated a SNP dataset with RAD sequencing to analyze population genetic structure, measure genetic diversity, and infer the processes that mediate genotype-phenotype dynamics. We investigated how patterns of genetic relatedness correspond with individual measures of color pattern along the coast, including testing for the role of hybridization in geographic regions where orange and purple phenotypic groups co-occur. We found no evidence that color-pattern polymorphism in the transition zone arose through recent hybridization or introgression. Instead, a strong pattern of genetic isolation by distance (IBD) indicates that color-pattern variation was retained through other processes such as ancestral color polymorphisms, ancient secondary contact or generated by novel mutations. We found that color phenotype changes along the Pacific coast more than would be expected from geographic distance alone. Combined, our results suggest the possibility of selective pressures acting on color pattern at a small geographic scale.
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Describing natural history of species is important because it would allow us to corroborate hypotheses about evolutionary biology and improve conservations plans. We describe the advertisement call, tadpole morphology, and other natural history aspects of the poison frog Andinobates daleswansoni, an endemic threatened species of the Colombian Andes. The advertisement call consists of multiple pulsed notes, with an average dominant frequency of 4052.81 ± 154.93 Hz. This call sounds similar to the call of other Andinobates frogs, but there are clear differences in spectral and temporal features. Tadpoles have a depressed body, low compressed dorsal and ventral tail fins with a rounded tip. The oral disc has a labial tooth row formula of 2(2)/3(1), and a gap in the marginal papillae of the lower lip, whose status as a synapomorphy for the group A. bombetes is discussed. Like other poison frogs, the diet of A. daleswansoni consists of small arthropods (Acari, Hymenoptera, Coleoptera) that individuals capture in leaflitter. We recorded tadpole transport by males to phytotelmata in the Elephant Ear plant (Xanthosoma robustum) which demonstrate that A. daleswansoni has a greater niche breadth for tadpole development than previously recorded. Acoustic interactions and physical fights observed during an agonistic behaviour on the part of two males of A. daleswansoni is similar to those recorded in other poison frogs and possible associated to the occupation of resources such as availability of prey items and places for breeding.
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Sexual imprinting—a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences—can generate reproductive barriers between species¹. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation1,2. However, in most models of speciation by sexual selection, divergent natural selection is also required; the latter acts to generate and maintain variation in the sexually selected trait or traits, and in the mating preferences that act upon them³. Here we demonstrate that imprinting, in addition to mediating female mate preferences, can shape biases in male–male aggression. These biases can act similarly to natural selection to maintain variation in traits and mate preferences, which facilitates reproductive isolation driven entirely by sexual selection. Using a cross-fostering study, we show that both male and female strawberry poison frogs (Oophaga pumilio) imprint on coloration, which is a mating trait that has diverged recently and rapidly in this species⁴. Cross-fostered females prefer to court mates of the same colour as their foster mother, and cross-fostered males are more aggressive towards rivals that share the colour of their foster mother. We also use a simple population-genetics model to demonstrate that when both male aggression biases and female mate preferences are formed through parental imprinting, sexual selection alone can (1) stabilize a sympatric polymorphism and (2) strengthen the trait–preference association that leads to behavioural reproductive isolation. Our study provides evidence of imprinting in an amphibian and suggests that this rarely considered combination of rival and sexual imprinting can reduce gene flow between individuals that bear divergent mating traits, which sets the stage for speciation by sexual selection.
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Recent reviews on sexual dichromatism in frogs included Mannophryne trinitatis as the only example they could find of dynamic dichromatism (males turn black when calling) within the family Aromobatidae and found no example of ontogenetic dichromatism in this group. We demonstrate ontogenetic dichromatism in M. trinitatis by rearing post-metamorphic froglets to near maturity: the throats of all individuals started as grey coloured; at around seven weeks, the throat became pale yellow in some, and more strongly yellow as development proceeded; the throats of adults are grey in males and variably bright yellow in females, backed by a dark collar. We demonstrated the degree of throat colour variability by analysing a large sample of females. The red: green (R:G) ratio ranged from ~1.1 to 1.4, reflecting variation from yellow to yellow/orange, and there was also variation in the tone and width of the dark collar, and in the extent to which the yellow colouration occurred posterior to the collar. Female M. trinitatis are known to be territorial in behaviour. We show a positive relationship between throat colour (R:G ratio) and escape performance, as a proxy for quality. Our field observations on Tobago’s M. olmonae showed variability in female throat colour and confirmed that males in this species also turn black when calling. Our literature review of the 20 Mannophryne species so far named showed that all females have yellow throats with dark collars, and that male colour change to black when calling has been reported in eight species; in the remaining 12 species, descriptions of males calling are usually lacking so far. We predict that both dynamic and ontogenetic sexual dichromatism are universal in this genus and provide discussion of the ecological role of dichromatism in this genus of predominantly diurnal, non-toxic frogs, with strong paternal care of offspring.
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Many organisms use conspicuous colour patterns to advertise their toxicity or unpalatability, a strategy known as aposematism. Despite the recognized benefits of this anti‐predator tactic, not all chemically defended species exhibit warning coloration. Here, we use a comparative approach to investigate which factors predict the evolution of conspicuousness in frogs, a group in which conspicuous coloration and toxicity have evolved multiple times. We extracted colour information from dorsal and ventral photos of 594 frog species for which chemical defence information was available. Our results show that chemically defended and diurnal species have higher internal chromatic contrast, both ventrally and dorsally, than chemically undefended and/or nocturnal species. Among species that are chemically defended, conspicuous coloration is more likely to occur if species are diurnal. Our results also suggest that the evolution of conspicuous colour is more likely to occur in chemically defended prey with smaller body size. We discuss potential explanations for this association and suggest that prey profitability (related to body size) could be an important force driving the macroevolution of warning signals. Many organisms use warning signals to advertise that they are unpalatable or toxic. This, however, does not always happen, and many chemically defended organisms do not advertise their toxicity. When are organisms more likely to advertise their defences? We used information on frog species and found that species that are chemically defended are more likely to be conspicuous (as expected). We also found that if species are already chemically defended, they are more likely to exhibit contrasting colourations if they are diurnal, and if they are relatively small. Our findings can help us understand under which conditions aposematism is more likely to evolve in nature.
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Muller's theory of warning color and mimicry, despite forming a textbook example of frequency-dependent selection, has rarely been demonstrated in the wild. This may be largely due to the practical and statistical difficulties of measuring natural selection on mobile prey species. Here we demonstrate that this selection acts in alpine beetle communities by using tethered beetles exposed to natural predators. Oreina gloriosa leaf beetles (Coleoptera: Chrysomelidae) possess chemical defense in the form of cardenolides, accompanied by what appears to be warning color in bright metallic blues and greens. Individuals that match the locally predominant color morph have increased survival, with odds of week-long survival increased by a factor of 1.67 over those that do not match. This corresponds to selection of 13% against foreign morphs. Such selection, acting in concert with variation in community composition, could be responsible for geographic variation in warning color. However, in the face of this purifying selection, the within-population polymorphism seen in many Oreina species remains paradoxical.
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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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Stynoski et al. introduce the dendrobatids, a charismatic group of frogs known for their colourful and often poisonous skin.
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The recognition that animals sense the world in a different way than we do has unlocked important lines of research in ecology and evolutionary biology. In practice, the subjective study of natural stimuli has been permitted by perceptual spaces, which are graphical models of how stimuli are perceived by a given animal. Because colour vision is arguably the best-known sensory modality in most animals, a diversity of colour spaces are now available to visual ecologists, ranging from generalist and basic models allowing rough but robust predictions on colour perception, to species-specific, more complex models giving accurate but context-dependent predictions. Selecting among these models is most often influenced by historical contingencies that have associated models to specific questions and organisms; however, these associations are not always optimal. The aim of this review is to provide visual ecologists with a critical perspective on how models of colour space are built, how well they perform and where their main limitations are with regard to their most frequent uses in ecology and evolutionary biology. We propose a classification of models based on their complexity, defined as whether and how they model the mechanisms of chromatic adaptation and receptor opponency, the nonlinear association between the stimulus and its perception, and whether or not models have been fitted to experimental data. Then, we review the effect of modelling these mechanisms on predictions of colour detection and discrimination, colour conspicuousness, colour diversity and diversification, and for comparing the perception of colour traits between distinct perceivers. While a few rules emerge (e.g. opponent log-linear models should be preferred when analysing very distinct colours), in general model parameters still have poorly known effects. Colour spaces have nonetheless permitted significant advances in ecology and evolutionary biology, and more progress is expected if ecologists compare results between models and perform behavioural experiments more routinely. Such an approach would further contribute to a better understanding of colour vision and its links to the behavioural ecology of animals. While visual ecology is essentially a transfer of knowledge from visual sciences to evolutionary ecology, we hope that the discipline will benefit both fields more evenly in the future.
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Umbers et al. introduce the biology of deimatic (frightening) visual displays used by animals. Copyright © 2015 Elsevier Ltd. All rights reserved.
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I studied the sex-limited red spots on the wings of male rubyspot damselflies (Hetaerina americana) in relation to territoriality and fitness in the wild. Both observational and experimental (wing spot manipulation) studies indicated that wing spots were selected through competition among males for mating territories, not through female choice or direct competition for females. Males with naturally or artificially large wing spots were more successful at holding territories and consequently mated at higher rates than males with relatively small wing spots. In contrast, sexual selection on male body size appeared to operate among nonterritorial males at the clasping stage of the mating sequence, perhaps because larger males were better at clasping females forcibly. Of four models proposed to explain the evolution of ornaments through territory competition, only the agonistic handicap model makes predictions consistent with the results of this study.
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