Multiple, recurring origins of aposematism and diet specialization in poison frogs

Abstract

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.

Fig. 1.

(a) Phylogeny of poison frogs. Species names in black refer to conspicuous and (as far as is known) toxic species. Names in gray refer to cryptic and nontoxic species. The tree shown is based on the parsimony analysis, but the likelihood tree (Fig. 2) is almost identical. The sister-group relationship of clades C and D was recovered in all three types of analyses. In the parsimony analysis, the sister-group relationship of clades B and C was equally supported, but this topology was not the best estimate under likelihood or Bayesian analysis. Neither alternative (clade C + D vs. clade B + C) is strongly supported by bootstrap proportions or Bayesian posterior probabilities. Parsimony bootstrap proportions are above each branch, and Bayesian posterior probabilities are below. *, a value of ≥95. (b) Previous molecular phylogeny of poison frogs (33). The difference between a and b is due to the degree of taxon sampling.

Fig. 2.

The likelihood topology, with gray boxes representing the species names shown in black on Fig. 1. The column of photos on the left shows representative cryptic and nontoxic species, and the column on the right shows conspicuous and toxic species (the toxicity of A. zaparo is unknown). The ant icons indicate two origins of specialized diet, and a possible third origin is indicated by a question mark.