Taste-rejection by predators and the evolution of unpalatability in prey

Aposematism is the association, in a prey organism, of the presence of a warning signal with unprofitability to predators. The origin of aposematism is puzzling, because of its predicted low probability of establishment in a population due to the prey's increased conspicuousness. Aposematism is a widespread trait in invertebrate taxa, but, in vertebrates, it is mostly evident in amphibians, reptiles, and fishes. Poison frogs (Dendrobatidae) are one of the most well known examples of the co-occurrence of warning coloration and toxicity. This monophyletic group of mostly diurnal leaf-litter Neotropical anurans has both toxic/colorful and palatable/cryptic species. Previous studies suggested a single origin of toxicity and warning coloration, dividing the family in two discrete groups of primitively cryptic and more derived aposematic frogs. Recent molecular phylogenetic analyses using mostly aposematic taxa supported this conclusion and proposed a single tandem origin of toxicity and conspicuous warning coloration. By using expanded taxon and character sampling, we reexamined the phylogenetic correlation between the origins of toxicity and warning coloration. At least four or five independent origins of aposematism have occurred within poison frogs; by using simulations, we rejected hypotheses of one, two, or three origins of aposematism (P < 0.002). We also found that diet specialization is linked with the evolution of aposematism. Specialization on prey, such as ants and termites, may have evolved independently at least two times.

The poison frogs (family Dendrobatidae) are terrestrial anuran amphibians displaying a wide range of coloration and toxicity. These frogs generally have been considered to be aposematic, but relatively little research has been carried out to test the predictions of this hypothesis. Here we use a comparative approach to test one prediction of the hypothesis of aposematism: that coloration will evolve in tandem with toxicity. Recently, we developed a phylogenetic hypothesis of the evolutionary relationships among representative species of poison frogs, using sequences from three regions of mitochondrial DNA. In our analysis, we use that DNA-based phylogeny and comparative analysis of independent contrasts to investigate the correlation between coloration and toxicity in the poison frog family (Dendrobatidae). Information on the toxicity of different species was obtained from the literature. Two different measures of the brightness and extent of coloration were used. (i) Twenty-four human observers were asked to rank different photos of each different species in the analysis in terms of contrast to a leaf-littered background. (ii) Color photos of each species were scanned into a computer and a computer program was used to obtain a measure of the contrast of the colors of each species relative to a leaf-littered background. Comparative analyses of the results were carried out with two different models of character evolution: gradual change, with branch lengths proportional to the amount of genetic change, and punctuational change, with all change being associated with speciation events. Comparative analysis using either method or model indicated a significant correlation between the evolution of toxicity and coloration across this family. These results are consistent with the hypothesis that coloration in this group is aposematic.

Understanding the early evolution of aposematic (warning) coloration has been a challenge for scientists, as a new conspicuous morph in a population of cryptic insects would have a high predation risk and would probably die out before local predators learnt to avoid it. Fisher presented the idea of aggregation benefit through the survival of related individuals; however, his theory has been strongly debated as the mechanisms that favour grouping have never been explored experimentally with the incorporation of detectability costs. Here we create a comprehensive 'novel world' experiment with the great tit (Parus major) as a predator to explore simultaneously the predation-related benefits and costs for aposematic aggregated prey, manipulating both group size and signal strength. Our results show that grouping would have been highly beneficial for the first aposematic prey individuals surrounded by naive predators, because (1) detectability risk increased only asymptotically with group size; (2) additional detectability costs due to conspicuous signals were marginal in groups; (3) even naive predators deserted the group after detecting unpalatability (dilution effect); and (4) avoidance learning of signal was faster in groups. None of these mechanisms require kin selection.