Passive accumulation of alkaloids in inconspicuously colored frogs refines the evolutionary paradigm of acquired chemical defenses

Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins. For most animals, the ability to deter predators is vital for survival. Some organisms, such as poison frogs, use bad tasting or toxic chemicals to ward off predators. In the 1990s, scientists discovered that poison frogs acquire their defensive alkaloid chemicals from the mites, ants and other arthropods they eat. Many poison frog species use bright or contrasting colors to advertise their defenses to predators; this strategy is known as ‘aposematism’. Aposematic frogs have evolved biochemical mechanisms to transport, store and even modify the alkaloid toxins. Although aposematism has evolved independently in three poison frog clades, most of the frogs in this family are dull-colored. These dull-colored frogs are generally assumed to not be able to accumulate alkaloid toxins from their diet. However, very little is known about how animals evolve to be able to use chemicals they eat