Skin Glands, Poison and Mimicry in Dendrobatid and Leptodactylid Amphibians

Laboratório de Biologia Celular, Instituto Butantan, São Paulo, Brazil.
Journal of Morphology (Impact Factor: 1.74). 03/2012; 273(3):279-90. DOI: 10.1002/jmor.11021
Source: PubMed


In amphibians, secretions of toxins from specialized skin poison glands play a central role in defense against predators. The production of toxic secretions is often associated with conspicuous color patterns that warn potential predators, as it is the case of many dendrobatid frogs, including Ameerega picta. This species resembles the presumably nontoxic Leptodactylus lineatus. This study tests for mimicry by studying the morphology and distribution of skin glands, components of skin secretion, and defensive behavior. Dorsal skin was studied histologically and histochemically, and skin secretions were submitted to sodium dodecyl sulfate polyacrylamide gel electrophoresis, reversed phase high performance liquid chromatography and assays for proteolytic activity. We found that poison glands in A. picta are filled with nonprotein granules that are rich in carbohydrates, while L. lineatus glands present protein granules. Accordingly, great amounts of proteins, at least some of them enzymes, were found in the poison of L. lineatus but not in that of A. picta. Both species differ greatly on profiles of gland distribution: In L. lineatus, poison glands are organized in clusters whose position coincides with colored elements of the dorsum. These regions are evidenced through a set of displays, suggesting that poison location is announced to predators through skin colors. In contrast, A. picta presents lower densities of glands, distributed homogeneously. This simpler profile suggests a rather qualitative than quantitative investment in chemical defense, in agreement with the high toxicity attributed to dendrobatids in general. Our data suggest that both species are toxic or unpalatable and transmit common warning signals to predators, which represents a case of Müllerian mimicry.

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Available from: Daniel Carvalho Pimenta
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    • "Reciprocal learned avoidance is a key tenet of Müllerian mimicry, and the results of Stuckert et al.[29] support the hypothesis of a Müllerian mimicry system—the first known in anurans. Other putative Müllerian complexes exist in anurans (e.g., mantellids [30], Amereega picta (Tschudi) and Leptodactylus lineatus (Schneider) [31], and among other members of the genus Ranitomeya[12]), but these have not been experimentally verified. "
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    ABSTRACT: Polytypism in aposematic species is unlikely according to theory, but commonly seen in nature. Ranitomeya imitator is a poison frog species exhibiting polytypic mimicry of three congeneric model species (R. fantastica, R. summersi, and two morphs of R. variabilis) across four allopatric populations (a "mimetic radiation"). In order to investigate chemical defenses in this system, a key prediction of Müllerian mimicry, we analyzed the alkaloids of both models and mimics from four allopatric populations. In this study we demonstrate distinct differences in alkaloid profiles between co-mimetic species within allopatric populations. We further demonstrate that R. imitator has a greater number of distinct alkaloid types than the model species and more total alkaloids in all but one population. Given that R. imitator is the more abundant species in these populations, R. imitator is likely driving the majority of predator-learned avoidance in these complexes. The success of Ranitomeya imitator as a putative advergent mimic may be a direct result of differences in alkaloid sequestration. Furthermore, we propose that automimicry within co-mimetic species is an important avenue of research.
    Full-text · Article · Apr 2014 · BMC Evolutionary Biology
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    • "Müllerian mimicry has been proposed for a number of anuran systems, including Ranitomeya imitator (Symula et al. 2001; Sherratt 2008; Brown et al. 2011), other complexes of Ranitomeya (Brown et al. 2011), mantellids (Schaefer et al. 2002), and between Amereega picta and Leptodactylus lineatus (Prates et al. 2012). However, no study to date has demonstrated reciprocal learned avoidance by predators of a shared morph within anura—a key component of Müllerian mimicry. "
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    ABSTRACT: The evolution of mimicry is one of the most powerful examples of evolution driven by natural selection; however it is rare in non-insect taxa and thus is understudied. Ranitomeya imitator underwent a ‘mimetic radiation’ and now mimics three congeneric model species (R. fantastica, R. summersi, and two morphs of R. variabilis), creating geographically distinct populations of the species, including four allopatric mimetic morphs. These complexes are thought to represent a case of Müllerian mimicry, but no prior empirical studies on learned avoidance by predators support this claim. In this study we used young chickens (Gallus domesticus) as naïve predators to determine if a co-mimetic morph of R. imitator and R. variabilis contribute to reciprocal learned avoidance by predators—a key component of Müllerian mimicry. Chickens exposed to either stimulus species demonstrated reciprocal learned avoidance; thus our results indicate that this complex functions as a Müllerian mimicry system. This study provides novel empirical evidence supporting predictions of the Müllerian mimicry hypothesis in anurans. Our study shows no difference between learned avoidance in stimuli frogs and a ‘novel’ morph of R. imitator that differed in both color and pattern, indicating that learned avoidance by predators may be generalized in this system. Generalized learning provides a plausible mechanism for the maintenance of both polytypic mimicry and the maintenance of intrapopulation phenotypic heterogeneity.
    Full-text · Article · Dec 2013 · Evolutionary Ecology
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    • "In contrast to the limited distribution of P. nordestina, P. hypochondrialis is found spread along biogeographically different habitats, which also include the rich Amazon rainforest biome. Taking into account that amphibian skin secretions are highly related to the type of environment in which a given species of frog inhabit (Prates et al., 2011), it can be anticipated that the molecules secreted by P. nordestina should be different from that described for P. hypochondrialis group. Several studies describing the biochemical characterization of the components from the skin secretion of Phyllomedusa genus have allowed the identification of biologically active peptides that are very similar to the mammalian hormones, neuropeptides, as well as the broad-spectrum cytolytic antimicrobial peptides (Conceição et al., 2006). "
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    ABSTRACT: The subfamily Phyllomedusinae has attracted a great interest of many researchers mainly due to the high diversity of these frog species and plethoraof pharmacological activities frequently observed for their skin secretions. Despite of this fact,mainly for new species, limited information is available regarding the molecular composition of these skin secretions and the cellular components involved in their production. Phyllomedusa nordestina is a recently described Brazilian frog species also popularlyknown as 'tree-frogs'. Aiming at contributing to the biological knowledge of this species, we show herethe geneexpression profile of this frog skin secretion using a global ESTs analysis of a cDNA library. The marked aspect of this analysis revealed a significant higher transcriptional level of the opioid peptide dermorphins in P. nordestina skin secretion than in Phyllomedusahypochondrialis, which is its closest related species, belonging both to the same phylogenetic group. Precursors of bioactive peptides as dermaseptins, phylloseptins, tryptophyllins, and bradykinin-like peptideswere also found in this library. Transcripts encoding proteins related to ordinary cellular functions and pathways werealso described. Some of them are chiefly involved in the production of the skin secretion. Taken together, the data reported hereconstitute a contribution tothe characterization of the molecular diversity of gene-encoded polypeptides with potential possibility of pharmacological exploitation. The transcriptional composition of the skin secretion may also help to give the necessary support for thedefinition ofP.nordestinaas a new species, which actually relies basically on frog morphological characteristics and geographical distribution.
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