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Despite rising interest among scientists for over two centuries, parental care behavior has not been as thoroughly studied in amphibians as it has in other taxa. The first reports of amphibian parental care date from the early 18th century, when Maria Sibylla Merian went on a field expedition in Suriname and reported frog metamorphs emerging from their mother's dorsal skin. Reports of this and other parental behaviors in amphibians remained descriptive for decades, often as side notes during expeditions with another purpose. However, since the 1980s, experimental approaches have proliferated, providing detailed knowledge about the adaptive value of observed behaviors. Today, we recognize more than 30 types of parental care in amphibians, but most studies focus on just a few families and have favored anurans over urodeles and caecilians. Here, we provide a synthesis of the last three centuries of parental care research in the three orders comprising the amphibians. We draw attention to the progress from the very first descriptions to the most recent experimental studies, and highlight the importance of natural history observations as a source of new hypotheses and necessary context to interpret experimental findings. We encourage amphibian parental care researchers to diversify their study systems to allow for a more comprehensive perspective of the behaviors that amphibians exhibit. Finally, we uncover knowledge gaps and suggest new avenues of research using a variety of disciplines and approaches that will allow us to better understand the function and evolution of parental care behaviors in this diverse group of animals.

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Chemical signaling in animals often plays a central role in eliciting a variety of responses during reproductive interactions between males and females. One of the best-known vertebrate courtship pheromone systems is sodefrin precursor-like factors (SPFs), a family of two-domain three-finger proteins with a female-receptivity enhancing function, currently only known from salamanders. The oldest divergence between active components in a single salamander species dates back to the Late Paleozoic, indicating that these proteins potentially gained a pheromone function earlier in amphibian evolution. Here, we combined whole transcriptome sequencing, proteomics, histology, and molecular phylogenetics in a comparative approach to investigate SPF occurrence in male breeding glands across the evolutionary tree of anurans (frogs and toads). Our study shows that multiple families of both terrestrially and aquatically reproducing frogs have substantially increased expression levels of SPFs in male breeding glands. This suggests that multiple anuran lineages make use of SPFs to complement acoustic and visual sexual signaling during courtship. Comparative analyses show that anurans independently recruited these proteins each time the gland location on the male’s body allowed efficient transmission of the secretion to the female’s nares.

The protection of offspring against predators and competitors is especially important in organisms using spatially separated breeding resources, impeding the offspring's chances to escape. One example of such isolated reproductive resources are phytotelmata (small water bodies in plant axils), exploited by the Neotropical poison frog Ranitomeya variabilis (Dendrobatidae) for both clutch and tadpole deposition. Because poison frog tadpoles are often cannibalistic, parents tend to avoid deposition with conspecifics. Previous studies have shown that this avoidance is based on chemical cues produced by conspecific tadpoles. Further, cues produced by phylogenetically less-related tadpoles (Bufonidae) were avoided for clutch but not tadpole depositions. We analyzed how the different responses to tadpole cues are triggered. We tested the reactions of parental R. variabilis to tadpole cues of species differing in two aspects: whether or not they are dendrobatids, and whether or not they reproduce in phytotelmata. We found that for clutch deposition, tadpole cues were always avoided, i.e., all tadpoles were treated by the frogs as if they pose a danger to the eggs. However, responses varied for tadpole depositions: while dendrobatid larvae living in phytotelmata were avoided, those breeding in streams were not. Non-poison frog tadpoles were ignored when associated with habitat other than phytotelmata, but they were preferred when living in phytotelmata. This suggests that both phylogeny and tadpole habitat are important triggers for the decisions made by R. variabilis. Only tadpoles using the same breeding resources are considered as relevant for the frog's own larvae (i.e., as a potential danger or food resource), while further decisions are related to evolutionary relationship.

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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