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opencc-zeroAug 2020View details →

UV reflectance in poison frog

We have identified strong UV reflectance in the white spots of only a single population of the polymorphic/polytypic poison frog species Oophaga sylvatica. As congeners (O. pumilio) are unable to view UV signals, it stands to reason that natural selection, or neutral processes are likely to be responsible for these signals. We employ visual modeling techniques to estimate the perception of these UV signals, and in a series of comparisons we show surprisingly minimal gains in frog contrast due to their addition.

opencc-zeroSep 2020View details →

The Influence of Environmental Variation on the Genetic Structure of a Poison Frog Distributed Across Continuous Amazonian Rainforest

Biogeographic barriers such as rivers have been shown to shape spatial patterns of biodiversity in the Amazon basin, yet relatively little is known about the distribution of genetic variation across continuous rainforest. Here, we characterize the genetic structure of the brilliant-thighed poison frog (Allobates femoralis) across an 880-km-long transect along the Purus-Madeira interfluve south of the Amazon river, based on 64 individuals genotyped at 7609 single-nucleotide polymorphism loci. A population tree and clustering analyses revealed 4 distinct genetic groups, one of which was strongly divergent. These genetic groups were concomitant with femoral spot coloration differences, which was intermediate within a zone of admixture between two of the groups. The location of these genetic groups did not consistently correspond to current ecological transitions between major forest types. A multimodel approach to quantify the relative influence of isolation-by-geographic distance (IBD) and isolation-by-environmental resistance (IBR) nevertheless revealed that, in addition to a strong signal of IBD, spatial genetic differentiation was explained by IBR primarily linked to dry season intensity (r2 = 8.4%) and canopy cover (r2 = 6.4%). We show significant phylogenetic divergence in the absence of obvious biogeographical barriers and that finer-scaled measures of genetic structure show patterns that are associated with environmental variables also known to predict the density of A. femoralis.

opencc-zeroSep 2020View details →

Data and code for: Male-male contest limits the expression of assortative mate preferences in a polymorphic poison frog

Co-divergence of sexual traits and mate preferences can lead to assortative mating and subsequently reproductive isolation. However, mate choice rarely operates without intrasexual competition, and the effects of the latter on speciation are often overlooked. Maintaining trait polymorphisms despite gene flow and limiting assortative female preferences for less-competitive male phenotypes are two important roles that male-male competition may play in the speciation process. Both roles rely on the assumption that male-male competition limits the expression of divergent female preferences. We tested this assumption in the highly color-polymorphic strawberry poison frog (Oophaga pumilio). Females prefer males of the local color, suggesting that reproductive isolation may be evolving among color morphs. However, this inference does not account for male-male competition, which is also color-mediated. We housed females with two differently-colored males, and compared reproductive patterns when the more attractive male was the territory holder versus when he was the non-territorial male. Females mated primarily with the territory winner, regardless of coloration, suggesting that when a choice must be made between the two, male territoriality overrides female preferences for male coloration. Our results highlight the importance of considering the combined effects of mate choice and intrasexual competition in shaping phenotypic divergence and speciation.

opencc-zeroSep 2020View details →

Data from: Ecological and social drivers of neighbor recognition and the dear enemy effect in a poison frog

Navigating social relationships frequently rests on the ability to recognize familiar individuals using phenotypic characteristics. Across diverse taxa, animals vary in their capacities for social recognition but the ecological and social sources of selection for recognition are often unclear. In a comparative study of two closely related species of poison frogs, we identified a species difference in social recognition of territory neighbors and investigated potential sources of selection underlying this difference. In response to acoustic playbacks, male golden rocket frogs (Anomaloglossus beebei) recognized the calls of neighbors and displayed a "dear enemy effect" by responding less aggressively to neighbors' calls than strangers' calls. In contrast, male Kai rocket frogs (Anomaloglossus kaiei) were equally aggressive to the calls of neighbors and strangers. This species difference in behavior is associated with key differences in reproductive ecology and characteristics of territories. Golden rocket frogs defend reproductive resources in the form of bromeliads, which is expected to create a threat asymmetry between neighbors and strangers favoring decreased aggression to neighbors. In contrast, Kai rocket frogs do not defend reproductive resources. Further, compared with Kai rocket frog territories, golden rocket frog territories occur at higher densities and are defended for longer periods of time, creating a more complex social environment with more opportunities for repeated but unnecessary aggression between neighbors, which should favor the ability to recognize and exhibit less aggression towards neighbors. These results suggest that differences in reproductive ecology can drive changes in social structure that select for social recognition.

opencc-zeroJan 2020View details →

The neural basis of tadpole transport in poison frogs

The occasional reversal of sex-typical behavior suggests that many of the neural circuits underlying behavior are conserved between males and females and can be activated in response to the appropriate social condition or stimulus. Most poison frog species (Family Dendrobatidae) exhibit male uniparental care, but flexible compensation has been observed in some species, where females will take over parental care duties when males disappear. We investigated hormonal and neural correlates of sex-typical and sex-reversed parental care in a typically male uniparental species, the Dyeing Poison Frog (Dendrobates tinctorius). We first characterized hormone levels and whole brain gene expression across parental care stages during sex-typical care. Surprisingly, hormonal changes and brain gene expression differences associated with active parental behavior in males were mirrored in their non-caregiving female partners. To further explore the disconnect between neuroendocrine patterns and behavior, we characterized hormone levels and neural activity patterns in females performing sex-reversed parental care. In contrast to hormone and gene expression patterns, we found that patterns of neural activity were linked to the active performance of parental behavior, with sex-reversed tadpole transporting females exhibiting neural activity patterns more similar to those of transporting males than non-caregiving females. We suggest that parallels in hormones and brain gene expression in active and observing parents are related to females' ability to flexibly take over parental care in the absence of their male partners.The occasional reversal of sex-typical behavior suggests that many of the neural circuits underlying behavior are conserved between males and females and can be activated in response to the appropriate social condition or stimulus. Most poison frog species (Family Dendrobatidae) exhibit male uniparental care, but flexible compensation has been observed in some species, where females will take over parental care duties when males disappear. We investigated hormonal and neural correlates of sex-typical and sex-reversed parental care in a typically male uniparental species, the Dyeing Poison Frog (Dendrobates tinctorius). We first characterized hormone levels and whole brain gene expression across parental care stages during sex-typical care. Surprisingly, hormonal changes and brain gene expression differences associated with active parental behavior in males were mirrored in their non-caregiving female partners. To further explore the disconnect between neuroendocrine patterns and behavior, we characterized hormone levels and neural activity patterns in females performing sex-reversed parental care. In contrast to hormone and gene expression patterns, we found that patterns of neural activity were linked to the active performance of parental behavior, with sex-reversed tadpole transporting females exhibiting neural activity patterns more similar to those of transporting males than non-caregiving females. We suggest that parallels in hormones and brain gene expression in active and observing parents are related to females' ability to flexibly take over parental care in the absence of their male partners.

opencc-zeroDec 2012View details →

Data from: Not everything is black and white: color and behavioral variation reveal a continuum between cryptic and aposematic strategies in a polymorphic poison frog

Aposematism and crypsis are often viewed as two extremes of a continuum of visual conspicuousness to predators. Theory predicts that behavioral and coloration conspicuousness should vary in tandem along the conspicuousness spectrum for antipredator strategies to be effective. Here we used visual modeling of contrast and behavioral observations to examine the conspicuousness of four populations of the granular poison frog, Oophaga granulifera, which exhibits almost continuous variation in dorsal color. The patterns of geographic variation in color, visual contrast, and behavior support a gradient of overall conspicuousness along the distribution of O. granulifera. Red and green populations, at the extremes of the color distribution, differ in all elements of color, contrast, and behavior, strongly reflecting aposematic and cryptic strategies. However, there is no smooth cline in any elements of behavior or coloration between the two extremes. Instead populations of intermediate colors attain intermediate conspicuousness by displaying different combinations of aposematic and cryptic traits. We argue that coloration divergence among populations may be linked to the evolution of a gradient of strategies to balance the costs of detection by predators and the benefits of learned aversion.

opencc-zeroDec 2016View details →

Data from: Diversification and convergence of aposematic phenotypes: truncated receptors and cellular arrangements mediate rapid evolution of coloration in harlequin poison frogs

Aposematic signals represent one of the classical systems to study evolution and, as such, they have received considerable empirical and theoretical investigation. Despite the extensive literature on aposematic coloration, much uncertainty remains about genetic changes responsible for the repeated evolution of similar signals in multiple lineages. Here, we study the diversification and convergence of coloration among lineages of aposematic harlequin poison frogs (O. histrionica complex). Our results suggest that different background phenotypes, showing different color and/or luminance contrast, have evolved independently at least twice in this group. We suggest that cellular arrangements are behind the striking diversity of color and patterns in this group and propose that differences in dorsal background color may be related to either or both, the presence/absence of xanthophores and the dispersion of melanosomes. Our genetic analyses support a role for the melanocortin receptor MC1R in melanosome aggregation, and we show evidence that two different mutations (∆433 and C432A) are responsible for the darker phenotypes that may display a more detectable, easier to learn, aposematic signal.

opencc-zeroDec 2012View details →

Data from: Hybridization promotes color polymorphism in the aposematic harlequin poison frog, Oophaga histrionica

Whether hybridization can be a mechanism that drives phenotypic diversity is a widely debated topic in evolutionary biology. In poison frogs (Dendrobatidae), assortative mating has been invoked to explain how new color morphs persist despite the expected homogenizing effects of natural selection. Here, we tested the complementary hypothesis that new morphs arise through hybridization between different color morphs. Specifically, we (1) reconstructed the phylogenetic relationships among the studied populations of a dart-poison frog to provide an evolutionary framework, (2) tested whether microsatellite allele frequencies of one putative hybrid population of the polymorphic frog O. histrionica are intermediate between O. histrionica and O. lehmanni, and (3) conducted mate-choice experiments to test whether putatively intermediate females prefer homotypic males over males from the other two populations. Our findings are compatible with a hybrid origin for the new morph and emphasize the possibility of hybridization as a mechanism generating variation in polymorphic species. Moreover, because coloration in poison frogs is aposematic and should be heavily constrained, our findings suggest that hybridization can produce phenotypic novelty even in systems where phenotypes are subject to strong stabilizing selection.

opencc-zeroDec 2017View details →

Data from: Male-male aggression is unlikely to stabilize a poison frog polymorphism

Phenotypic polymorphism is common in animals, and the maintenance of multiple phenotypes in a population requires forces that act against homogenizing drift and selection. Male-male competition can contribute to the stability of a polymorphism when males compete primarily with males of the same phenotype. In and around a contact zone between red and blue lineages of the poison frog Oophaga pumilio, we used simulated territorial intrusions to test the non-exclusive predictions that males would direct more aggression toward males of (i) their own phenotype and/or (ii) the phenotype that is most common in their population. Males in the monomorphic red and blue populations that flank the contact zone were more aggressive toward simulated intruders that matched the local coloration. However, males in the two polymorphic populations biased aggression toward neither their own color nor the color most common in their population. In sympatry, the rarer color morph gains no advantage via reduced male-male aggression from territorial males in these O. pumilio populations, and so male aggression seems unlikely to stabilize color polymorphism on its own. More broadly, these results suggest that the potential for divergent male aggression biases to maintain phenotypic diversity depends on the mechanism(s) that generate the biases and the degree to which these mechanisms persist in sympatry.

opencc-zeroDec 2010View details →

Data from: Poison frog colors are honest signals of toxicity, particularly for bird predators

Antipredator defenses and warning signals typically evolve in concert. However, the extensive variation across taxa in both these components of predator deterrence, and the relationship between them, are poorly understood. Here we test whether there is a predictive relationship between visual conspicuousness and toxicity levels across 10 populations of the color polymorphic strawberry poison frog, Dendrobates pumilio. Using a mouse-based toxicity assay, we find extreme variation in toxicity between frog populations. This variation is significantly positively correlated with frog coloration brightness, a viewer-independent measure of visual conspicuousness (i.e. total reflectance flux). We also examine conspicuousness from the view of three potential predator taxa, as well as conspecific frogs, using taxon-specific visual detection models and three natural background substrates. We find very strong positive relationships between frog toxicity and conspicuousness for bird-specific perceptual models. Weaker but still positive correlations are found for crab and D. pumilio conspecific visual perception, while frog coloration as viewed by snakes is not related to toxicity. These results suggest that poison frog colors can be honest signals of prey unpalatability to predators, and that birds in particular may exert selection on aposematic signal design.

opencc-zeroDec 2014View details →

Data from: Mimetic divergence and the speciation continuum in the mimic poison frog Ranitomeya imitator

While divergent ecological adaptation can drive speciation, understanding the factors that facilitate or constrain this process remains a major goal in speciation research. Here, we study two mimetic transition zones in the poison frog Ranitomeya imitator, a species that has undergone a Müllerian mimetic radiation to establish four morphs in Peru. We find that mimetic morphs are strongly phenotypically differentiated, producing geographic clines with varying widths. However, distinct morphs show little neutral genetic divergence, and landscape genetic analyses implicate isolation-by-distance as the primary determinant of among-population genetic differentiation. Mate choice experiments suggest random mating at the transition zones, although certain allopatric populations show a preference for their own morph. We present evidence that this preference may be mediated by color-pattern specifically. These results contrast with an earlier study of a third transition zone, in which a mimetic shift was associated with reproductive isolation. Overall, our results suggest that the three known mimetic transition zones in R. imitator reflect a speciation continuum, which we have characterized at the geographic, phenotypic, behavioral, and genetic level. We discuss possible explanations for variable progress toward speciation, suggesting that multifarious selection on both mimetic color-pattern and body size may be responsible for generating reproductive isolation.

FIGURE 6 in A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia

FIGURE 6. Advertisement call of Ranitomeya tolimense. A. Audiospectrogram of a call with three notes. B. Oscillogram of the three notes showing the pulses.

FIGURE 5 in A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia

FIGURE 5. Tadpole of Ranitomeya tolimense (CZUT-A 991). (A) Lateral view, stage 25 (Gosner, 1960). Scale equals 5 mm. (B) Mouth parts. Scale equals 1mm.

FIGURE 2 in A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia

FIGURE 2. Male nurse frog (CZUT-A 990) with a tadpole over his back at the type locality. Photo: Victor Luna.

FIGURE 1 in A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia

FIGURE 1. Ranitomeya tolimense, new species. Lateral view showing color pattern. CZUT-A 989 adult female, SVL 17.94 mm. Photo: Manuel H. Bernal.

opennotspecifiedDec 2009View details →

FIGURE 12. Ameerega petersi, A in Complicated histories: three new species of poison frogs of the genus Ameerega (Anura: Dendrobatidae) from north-central Peru

FIGURE 12. Ameerega petersi, A. smaragdina, and A. bassleri. (a) A. petersi from Puerto Inca, Huánuco, Peru; (b) A. petersi from Tournavista, Huánuco, Peru; (c,d) A. smaragdina from Pan de Azucar, Pasco, Peru (photo 'd' by K. Summers); (e-h) A. bassleri from 8.6 km E of San José de Sisa, San Martín, Peru; (i-o) A. bassleri from 7 km NW of Saposoa, San Martín, Peru.

opennotspecifiedDec 2009View details →

FIGURE 15 in Complicated histories: three new species of poison frogs of the genus Ameerega (Anura: Dendrobatidae) from north-central Peru

FIGURE 15. Ameerega pepperi and habitat photos for the new species in this paper. (a,e) A. pepperi from Chumanza, San Martín, Peru (photo 'a' by M. Pepper); (b-d) A. pepperi from Río Abiseo near Huicungo, San Martín, Peru; (f,g) A. pepperi from 6.3 km N of Campanilla, San Martín, Peru; (h) type locality of A. ignipedis, a geothermal stream flowing out of the Serranía de Contamana. The entire type series (as well as one A. yoshina metamorph) was found in the forest adjacent to the stream or among the plants growing in the stream banks. (i) type locality of A. pepperi near San Francisco, San Martín, Peru. (j) Quebrada Pacuyacu near Callanayacu. Three A. yoshina paratypes (MUSM 26985- 26987) were collected from amongst the rocks and vegetation alongside the stream.