Multilevel perspective reveals heterogeneous acoustic adaptation in the poison-dart frog Oophaga pumilio

Abstract

Acoustic trait divergence may play an important role in facilitating speciation in many species, have been shown to be sensitive to natural selection due to habitat type and background noise. Despite this, heterogeneous acoustic adaptation has remained understudied. This article uses a Bayesian hierarchical (multilevel) analysis of acoustic calls recorded in Islas Bastimentos and Solarte in the Bocas del Toro Archipelago to understand heterogeneous acoustic adaptation in the strawberry poison-dart frog (Oophaga pumilio). We find that both mean and standard deviation of peak frequency (average call frequency), and the mean and standard deviation of repertoire width (intraindividual variability) shift and increase as a result of heterogeneous adaptation in Bastimentos. In silico experiments indicate that simulated females were able to assortatively mate with both Bastimentos and Solarte males with 85% accuracy based on only 4 calls; the eco-evolutionary implications of this are discussed. Since acoustic traits allow for both intra- and interindividual variability, heterogeneous acoustic adaptation can become incredibly complex. By describing a model of heterogeneous acoustic adaptation for simple calls, we propose an interpretation of population-level distributions of acoustic phenotypes that provides information not only about the average direction and variability of selection, but also about the average patch size (or periodicity in the case of temporal heterogeneity) and variability in patch size (or temporal unpredictability), and contextualize this model in terms of its application to Bastimentos. The results found here differ from a previous analysis of the archipelago, underscoring the importance of multilevel models in understanding acoustic adaptation. Finally, the conservation implications of heterogeneous acoustic adaptation are considered as an analogy to acoustic divergence between Bastimentos and Solarte.