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opencc-zeroMay 2020View details →

Data from: A ketocarotenoid-based color polymorphism in the Sira poison frog Ranitomeya sirensis indicates novel gene interactions underlying aposematic signal variation

The accumulation of red ketocarotenoids is an important component of coloration in many organisms, but the underlying mechanisms are poorly understood. In some organisms, ketocarotenoids are sequestered from the diet and can accumulate when enzymes responsible for carotenoid breakdown are disrupted. In other organisms, ketocarotenoids are formed endogenously from dietary precursors via oxidation reactions carried out by carotenoid ketolase enzymes. Here, we study the genetic basis of carotenoid coloration in an amphibian. We demonstrate that a red/yellow polymorphism in the dendrobatid poison frog Ranitomeya sirensis is due to the presence/absence of ketocarotenoids. Using whole-transcriptome sequencing of skins and livers, we found that a transcript encoding a cytochrome P450 enzyme (CYP3A80) is expressed 3.4-fold higher in livers of red frogs versus yellow. As CYP3A enzymes are known carotenoid ketolases in other organisms, our results point to CYP3A80 as a strong candidate for a carotenoid ketolase in amphibians. Furthermore, in red frogs, the transcript encoding the carotenoid cleavage enzyme BCO2 is expressed at a low level or as a splice variant lacking key catalytic amino acids. This suggests that BCO2 function may be disrupted in red frogs, providing a mechanism whereby the accumulation of ketocarotenoids and their dietary precursors may be enhanced.

opencc-zeroNov 2023View details →

Binding and sequestration of poison frog alkaloids by a plasma globulin

Alkaloids are important bioactive molecules throughout the natural world, and in many animals, they serve as a source of chemical defense against predation. Dendrobatid poison frogs bioaccumulate alkaloids from their diet to make themselves toxic or unpalatable to predators. Despite the proposed roles of plasma proteins as mediators of alkaloid trafficking and bioavailability, the responsible proteins have not been identified. We use chemical approaches to show that a ~50 kDa plasma protein is the principal alkaloid binding molecule in blood from poison frogs. Proteomic and biochemical studies establish this plasma protein to be liver-derived alkaloid-binding globulin (ABG) that is a member of the serine-protease inhibitor (serpin) family. In addition to alkaloid binding activity, ABG sequesters and regulates the bioavailability of "free" plasma alkaloids in vitro. Unexpectedly, ABG is not related to saxiphilin or albumin but instead exhibits sequence and structural homology to mammalian hormone carriers and amphibian biliverdin binding proteins. Alkaloid-binding globulin (ABG) represents a new small molecule binding functionality in serpin proteins, a novel mechanism of plasma alkaloid transport in poison frogs, and more broadly points towards serpins acting as tunable scaffolds for small molecule binding and transport across different organisms.

opencc-zeroDec 2023View details →

Supplementary material from: Deep divergences among inconspicuous clades of Epipedobates poison frogs

Poison frogs (Dendrobatidae) are famous for their aposematic species, having a combination of diverse color patterns and defensive skin toxins, yet most species in this family are inconspicuously colored and considered non-aposematic. Epipedobates is among the youngest genus-level clades of Dendrobatidae that includes both aposematic and inconspicuous species. Using Sanger-sequenced mitochondrial and nuclear markers, we demonstrate deep genetic divergences among inconspicuous species of Epipedobates but relatively shallow genetic divergences among conspicuous species. Our phylogenetic analysis includes broad geographic sampling of the inconspicuous lineages typically identified as E. boulengeri and E. espinosai, which reveals two putative new species, one in west-central Colombia (E. sp. 1) and the other in north-central Ecuador (E. aff. espinosai). We conclude that E. darwinwallacei is a junior subjective synonym of E. espinosai. We also clarify the geographic distributions of inconspicuous Epipedobates species including the widespread E. boulengeri. We provide a qualitative assessment of the phenotypic diversity in each nominal species, with a focus on the color and pattern of inconspicuous species. We conclude that Epipedobates contains eight known valid species, six of which are inconspicuous. A relaxed molecular clock analysis suggests that the most recent common ancestor of Epipedobates is ~11.1 million years old, which nearly doubles previous estimates. Last, genetic information points to a center of species diversity in the Chocó at the southwestern border of Colombia with Ecuador.

opencc-zeroJun 2024View details →

Physiological state matching in a pair bonded poison frog

More than a century ago, Charles Darwin hypothesized that the empathy-like phenotype is a phylogenetically widespread phenomenon. This idea remains contentious, due to the challenges of empirically examining emotions, and few investigations among non-mammalian vertebrates. We provide support for Darwin's hypothesis by discovering partial evidence for the most ancestral form of empathy, emotional contagion (i.e., matching another individual's emotional state), in the pair bonding mimetic poison frog, Ranitomeya imitator. We found that male corticosterone, a physiological biomarker of stress, positively correlates with female partners in experimental and semi-natural conditions. This does not appear to coincide with behavioral state-matching. However, it is specific to female partners relative to familiar female non-partners, and is independent of effects that commonly confound studies on emotional contagion. Furthermore, this physiological state-matching is irrespective of partnership longevity or lifetime reproductive output. These results physiologically indicate socially selective emotional contagion in a monogamous amphibian, and paradigms that elicit coinciding neural and behavioral indicators and morphogenic co-variation are needed for further corroboration. Further studies on ancestral forms of empathy in non-mammalian vertebrates are warranted.

Fig. 78 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 78. Graphic summary of the proposed taxonomy of Dendrobatoidea.

Fig. 77 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 77. Graphic summary of the proposed higher-level taxonomy of Athesphatanura.

Fig. 45. Character 60 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 45. Character 60, dark lower lip line. State

Fig. 34. Character 49, pale paracloacal mark. State 1 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 34. Character 49, pale paracloacal mark. State 1, present (degranvillei, AMNH 90880).

Fig. 32. Character 30, tarsal fringe. State 1 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 32. Character 30, tarsal fringe. State 1, present (Megaelosia goeldii, AMNH 103950).

Fig. 38. Character 53, dorsolateral stripe B. State 1 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 38. Character 53, dorsolateral stripe B. State 1, present (femoralis, AMNH 140646).

Fig. 29. Character 22 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 29. Character 22, male supracarpal pad

Fig. 27. Character 19 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 27. Character 19, metacarpal ridge. State

Fig. 14 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 14. Hypothesized phylogeny of anurans, redrawn from Lynch (1973).

Fig. 15 in PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE)

Fig. 15. Hypothesized phylogeny of neobatrachians, redrawn from Ford and Cannatella (1993).

opencc-by-4.0Dec 2019View details →

Fig. 2 in The Blue Dyeing Poison-Dart Frog, Dendrobates tinctorius (Dendrobates azureus, Hoogmoed 1969): extant in Suriname based on a rapid survey

Fig. 2. Dendrobates tinctorius from Sipaliwini savanna, Suriname.

opencc-zeroDec 2018View details →

Data from: Molecular physiology of chemical defenses in a poison frog

Poison frogs sequester small molecule lipophilic alkaloids from their diet of leaf litter arthropods for use as chemical defenses against predation. Although the dietary acquisition of chemical defenses in poison frogs is well-documented, the physiological mechanisms of alkaloid sequestration has not been investigated. Here, we used RNA sequencing and proteomics to determine how alkaloids impact mRNA or protein abundance in the Little Devil Frog (Oophaga sylvatica) and compared wild caught chemically defended frogs to laboratory frogs raised on an alkaloid-free diet. To understand how poison frogs move alkaloids from their diet to their skin granular glands, we focused on measuring gene expression in the intestines, skin, and liver. Across these tissues, we found many differentially expressed transcripts involved in small molecule transport and metabolism, as well as sodium channels and other ion pumps. We then used proteomic approaches to quantify plasma proteins, where we found several protein abundance differences between wild and laboratory frogs, including the amphibian neurotoxin binding protein saxiphilin. Finally, because many blood proteins are synthesized in the liver, we used thermal proteome profiling as an untargeted screen for soluble proteins that bind the alkaloid decahydroquinoline. Using this approach, we identified several candidate proteins that interact with this alkaloid, including saxiphilin. These transcript and protein abundance patterns suggest the presence of alkaloids influences frog physiology and that small molecule transport proteins may be involved in toxin bioaccumulation in dendrobatid poison frogs.

opencc-zeroDec 2019View details →

Mechanisms of Convergent Egg Provisioning in Poison Frogs

Parental provisioning of offspring with physiological products (nursing) occurs in many animals, yet little is known about the neuroendocrine basis of nursing in non-mammalian species. Within amphibians, maternal provisioning has evolved multiple times, with mothers of some species feeding unfertilized eggs to their developing offspring until tadpoles complete metamorphosis. We conducted field studies in Ecuador and Madagascar to ask whether convergence at the behavioral level provides similar benefits to offspring and relies on shared neural mechanisms in dendrobatid and mantellid poison frogs. At an ecological level, we found that nursing allows poison frogs to provide chemical defenses to their tadpoles in both species. At the neural level, nursing was associated with increased activity in the lateral septum and preoptic area, demonstrating recruitment of shared brain regions in the convergent evolution of nursing within frogs and across vertebrates. In contrast, only mantellids showed increased oxytocin neuron activity akin to that in nursing mammals, suggesting evolutionary versatility in molecular mechanisms. Our findings demonstrate that maternal provisioning provides similar potential benefits to offspring and relies on similar brain regions in poison frog species with convergently evolved toxicity and maternal care.

opencc-zeroSep 2021View details →

Data from: The evolution of polymorphism in the warning coloration of the Amazonian poison frog Adelphobates galactonotus

While intraspecific variation in aposematic signals can be selected for by different predatory responses, their evolution is also contingent on other processes shaping genetic variation. We evaluate the relative contributions of selection, geographic isolation and random genetic drift to the evolution of aposematic color polymorphism in the poison frog Adelphobates galactonotus, distributed throughout eastern Brazilian Amazonia. Dorsal coloration was measured for 111 individuals and genetic data were obtained from 220 individuals at two mitochondrial genes (mtDNA) and 7963 Single Nucleotide Polymorphisms (SNPs). Four color categories were described (brown, blue, yellow, orange) and our models of frog and bird visual systems indicated that each color was distinguishable for these taxa. Using outlier and correlative analyses we found no compelling genetic evidence for color being under divergent selection. A time-calibrated mtDNA tree suggests that the present distribution of dorsal coloration resulted from processes occurring during the Pleistocene. Separate phylogenies based on SNPs and mtDNA resolved the same well supported clades, each containing different colored populations. Ancestral character state analysis provided some evidence for evolutionary transitions in color type. Genetic structure was more strongly associated with geographic features, than color category, suggesting that the distribution of color is explained by localized processes. Evidence for geographic isolation together with estimates of low effective population size implicates drift as playing a key role in color diversification. Our results highlight the relevance of considering the neutral processes involved with the evolution of traits with important fitness consequences.

opencc-zeroNov 2022View details →

Poison frog dietary preference depends on prey type and alkaloid load

The ability to acquire chemical defenses through the diet has evolved across several major taxa. Chemically defended organisms may need to balance chemical defense acquisition and nutritional quality of prey items. However, these dietary preferences and potential trade-offs are rarely considered in the framework of diet-derived defenses. Poison frogs (Family Dendrobatidae) acquire defensive alkaloids from their arthropod diet of ants and mites, although their dietary preferences have never been investigated. We conducted prey preference assays with the Dyeing Poison frog (Dendrobates tinctorius) to test the hypothesis that alkaloid load and prey traits influence frog dietary preferences. We tested size preferences (big versus small) within each of four prey groups (ants, beetles, flies, and fly larvae) and found that frogs preferred interacting with smaller prey items of the fly and beetle groups. Frog taxonomic prey preferences were also tested as we experimentally increased their chemical defense load by feeding frogs decahydroquinoline, an alkaloid compound similar to those naturally found in their diet. Contrary to our expectations, overall preferences did not change during alkaloid consumption, as frogs across groups preferred fly larvae over other prey. Finally, we assessed the protein and lipid content of prey items and found that small ants have the highest lipid content while large fly larvae have the highest protein content. Our results suggest that consideration of toxicity and prey nutritional value are important factors in understanding the evolution of acquired chemical defenses and niche partitioning as a whole.