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      Decoding and Discrimination of Chemical Cues and Signals: Avoidance of Predation and Competition during Parental Care Behavior in Sympatric Poison Frogs

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          Abstract

          The evolution of chemical communication and the discrimination between evolved functions (signals) and unintentional releases (cues) are among the most challenging issues in chemical ecology. The accurate classification of inter- or intraspecific chemical communication is often puzzling. Here we report on two different communication systems triggering the same parental care behavior in the poison frog Ranitomeya variabilis. This species deposits its tadpoles and egg clutches in phytotelmata and chemically recognizes and avoids sites with both predatory conspecific and non-predatory heterospecific tadpoles (of the species Hyloxalus azureiventris). Combining chemical analyses with in-situ bioassays, we identified the molecular formulas of the chemical compounds triggering this behavior. We found that both species produce distinct chemical compound combinations, suggesting two separate communication systems. Bringing these results into an ecological context, we classify the conspecific R. variabilis compounds as chemical cues, advantageous only to the receivers (the adult frogs), not the emitters (the tadpoles). The heterospecific compounds, however, are suggested to be chemical signals (or cues evolving into signals), being advantageous to the emitters (the heterospecific tadpoles) and likely also to the receivers (the adult frogs). Due to these assumed receiver benefits, the heterospecific compounds are possibly synomones which are advantageous to both emitter and receiver ‒ a very rare communication system between animal species, especially vertebrates.

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          Most cited references 16

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          In silico fragmentation for computer assisted identification of metabolite mass spectra

          Background Mass spectrometry has become the analytical method of choice in metabolomics research. The identification of unknown compounds is the main bottleneck. In addition to the precursor mass, tandem MS spectra carry informative fragment peaks, but the coverage of spectral libraries of measured reference compounds are far from covering the complete chemical space. Compound libraries such as PubChem or KEGG describe a larger number of compounds, which can be used to compare their in silico fragmentation with spectra of unknown metabolites. Results We created the MetFrag suite to obtain a candidate list from compound libraries based on the precursor mass, subsequently ranked by the agreement between measured and in silico fragments. In the evaluation MetFrag was able to rank most of the correct compounds within the top 3 candidates returned by an exact mass query in KEGG. Compared to a previously published study, MetFrag obtained better results than the commercial MassFrontier software. Especially for large compound libraries, the candidates with a good score show a high structural similarity or just different stereochemistry, a subsequent clustering based on chemical distances reduces this redundancy. The in silico fragmentation requires less than a second to process a molecule, and MetFrag performs a search in KEGG or PubChem on average within 30 to 300 seconds, respectively, on an average desktop PC. Conclusions We presented a method that is able to identify small molecules from tandem MS measurements, even without spectral reference data or a large set of fragmentation rules. With today's massive general purpose compound libraries we obtain dozens of very similar candidates, which still allows a confident estimate of the correct compound class. Our tool MetFrag improves the identification of unknown substances from tandem MS spectra and delivers better results than comparable commercial software. MetFrag is available through a web application, web services and as java library. The web frontend allows the end-user to analyse single spectra and browse the results, whereas the web service and console application are aimed to perform batch searches and evaluation.
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            Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates.

             T. Wyatt (2010)
            Pheromones have been found in species in almost every part of the animal kingdom, including mammals. Pheromones (a molecule or defined combination of molecules) are species-wide signals which elicit innate responses (though responses can be conditional on development as well as context, experience, and internal state). In contrast, signature mixtures, in invertebrates and vertebrates, are variable subsets of molecules of an animal's chemical profile which are learnt by other animals, allowing them to distinguish individuals or colonies. All signature mixtures, and almost all pheromones, whatever the size of molecules, are detected by olfaction (as defined by receptor families and glomerular processing), in mammals by the main olfactory system or vomeronasal system or both. There is convergence on a glomerular organization of olfaction. The processing of all signature mixtures, and most pheromones, is combinatorial across a number of glomeruli, even for some sex pheromones which appear to have 'labeled lines'. Narrowly specific pheromone receptors are found, but are not a prerequisite for a molecule to be a pheromone. A small minority of pheromones act directly on target tissues (allohormone pheromones) or are detected by non-glomerular chemoreceptors, such as taste. The proposed definitions for pheromone and signature mixture are based on the heuristic value of separating these kinds of chemical information. In contrast to a species-wide pheromone, there is no single signature mixture to find, as signature mixtures are a 'receiver-side' phenomenon and it is the differences in signature mixtures which allow animals to distinguish each other.
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              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. © 2011 by The University of Chicago.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 July 2015
                2015
                : 10
                : 7
                Affiliations
                [1 ]Department of Biogeography, Trier University, Trier, Germany
                [2 ]Department of Effect-Directed Analysis, Helmholtz Centre for Environmental Research, Leipzig, Germany
                University of Arkansas, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: LMS WB MK TS SL. Performed the experiments: LMS MK TS. Analyzed the data: LMS MK TS. Wrote the paper: LMS SL MK.

                [¤]

                Current address: Amphibian Evolution Lab, Vrije Universiteit Brussel, Brussels, Belgium

                Article
                PONE-D-15-09571
                10.1371/journal.pone.0129929
                4488855
                26132416

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Page count
                Figures: 3, Tables: 2, Pages: 17
                Product
                Funding
                This work was supported by Studienstiftung des Deutschen Volkes https://www.studienstiftung.de/; Deutsche Forschungsgemeinschaft LO 1681/1-1 http://www.dfg.de/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
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                All relevant data are within the paper and its Supporting Information files.

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