Co-option of ancestral signal elements in the evolution of a cooperative parental behavior

Abstract

AbstractThe emergence of complex social interactions is predicted to be an important selective force in the diversification of communication systems. Parental care presents a key social context in which to study the evolution of novel signals, as care often requires communication and behavioral coordination between parents and is an evolutionary stepping-stone towards increasingly complex social systems. Anuran amphibians (frogs and toads) are a classic model of acoustic communication and the vocal repertoires of many species have been characterized in the contexts of advertisement, courtship, and aggression; yet quantitative descriptions of calls elicited in the context of parental care are lacking. The biparental poison frog,Ranitomeya imitator, exhibits a remarkable parenting behavior in which females, cued by the calls of their male partners, feed tadpoles unfertilized eggs. Here, we characterized and compared calls across three social contexts, for the first time including a parental care context. We found that egg feeding calls share some properties with both advertisement and courtship calls but also had unique properties. Multivariate analysis revealed high classification success for advertisement and courtship calls but misclassified nearly half of egg feeding calls as either advertisement or courtship calls, suggesting additional signal modalities play a role in parental communication. Egg feeding and courtship calls both contained less identity information than advertisement calls, as expected for signals used in close-range communication where uncertainty about identity is low. Taken together, egg feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.Significance StatementParental care has evolved independently in every major animal lineage and represents a major step in the evolution of complex sociality. Communication systems may need to increase in complexity. To explore these ideas, we characterized calls associated with trophic egg feeding, a unique cooperative parental behavior in the biparental mimic poison frog and compared them to calls associated with mate attraction (advertisement and courtship calls). Our analysis revealed some distinct, but many shared properties of signals elicited during egg feeding, suggesting that signals deployed in a novel social context evolve via modification and recombination of existing signals. These findings deepen our understanding of the relationship between complexity of social and communication systems.