Evidence for a Parabasalian Gut Symbiote in Egg-Feeding Poison Frog Tadpoles in Peru

Abstract

We report preliminary evidence of a symbiotic parabasalian protist in the guts of Peruvian mimic poison frog (Ranitomeya imitator) tadpoles. This species has biparental care and egg-feeding of tadpoles, while the related R. variabilis consumes the ancestral detritus diet in their nursery pools. Each species’ diet was experimentally switched, in the field and lab. Analyses of gut gene expression revealed elevated expression of proteases in the R. imitator field egg-fed treatment. These digestive proteins came from parabasalians, a group of protists known to form symbiotic relationships with hosts that enhance digestion. Genes that code for these digestive proteins are not present in the R. imitator genome, and phylogenetic analyses indicate that these mRNA sequences are from parabasalians. Bar-coding analyses of the tadpole microbiomes further confirmed this discovery. Our findings indicate the presence of parabasalian symbiotes in the intestines of the R. imitator tadpoles, that may aid the tadpoles in protein/lipid digestion in the context of an egg diet. This may have enabled the exploitation of a key ecological niche, allowing R. imitator to expand into an area with ecologically similar species (e.g., R. variabilis and R. summersi). In turn, this may have enabled a Müllerian mimetic radiation, one of only a few examples of this phenomenon in vertebrates.