Evolution of acoustic signals associated with cooperative parental behavior in a poison frog

Abstract

The 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 toward 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. 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 and additional signal modalities may be used. Taken together, egg-feeding calls likely borrowed and recombined elements of both ancestral call types to solicit a novel, context-dependent parenting response.

Keywords: animal communication; anuran; cooperation; parental care; social context.

Fig. 1.

Phylogeny, redrawn and trimmed from Brown et al. (28), illustrating the diversification of parental care behaviors in Ranitomeya and other representative species of Dendrobatidae (note: branch lengths are not meaningful and only a subset of representative species outside of Ranitomeya are shown). The ancestral state of this family is male parental care; cooperative biparental care with egg feeding (gold branches) is a highly derived state occurring only in the Ranitomeya vanzolinii group. References for character states are provided in Dataset S1.

Fig. 2.

Vocalizations have unique spectral profiles across social contexts. Spectrograms and associated power spectra of representative (A) advertisement call; (B) courtship call; and (C) egg feeding call of R. imitator (photo, Top). Calls were visualized in Raven Pro v. 1.6.1 (31) using the Hann window, 256 pt frequency resolution. The courtship and egg feeding call power spectra show the two forms of increased frequency bandwidth: broader dominant frequency peak (B) or a fundamental frequency that is at a higher relative amplitude (C). See SI Appendix, Fig. S1 for variations on these patterns. Photo by Anton Sorokin, antonsrkn@gmail.com.

Fig. 3.

Acoustic properties of R. imitator vocalizations vary between advertisement, courtship, and egg feeding calls. Plots depict distributions of four acoustic properties by call type: (A) Pulse duration; (B) log10 (Pulse interval); (C) log10 (Dominant frequency); and (D) log10 (Bandwidth 90%). Color of dots corresponds to seven unique males in the sample. Asterisks indicate significance levels for Tukey–HSD post hoc contrasts.

Fig. 4.

Classification success of vocalizations based on acoustic properties exceeds chance levels, despite considerable overlap. Classification success was significantly above chance (33%) for all call types: 82.9% for advertisement calls, 73.5% for courtship calls (73.5%), and 57.1% for egg feeding calls. Courtship calls were equally likely to be misclassified as advertisement (13.2%) or egg feeding calls (13.2%), and egg feeding calls were equally likely to be misclassified as advertisement (21.4%) or courtship calls (21.4%). Plot of R. imitator calls in two-dimensional space defined by the first two discriminant functions of a linear discriminant function analysis (DFA). Calls are clustered by call type (advertisement, courtship, and egg feeding) with centroids (large points) and 95% CIs (ellipses) depicted for each type.