Going silent? Evidence for independent losses of acoustic communication in tree crickets (Insecta, Orthoptera, Grylloidea, Oecanthidae)

Abstract

Singing is a key innovation that drives the diversification of crickets. However, acoustic-related traits have not been investigated in a broad phylogenetic context, making the evolution of acoustic communication enigmatic. To explore the evolution and regression of singing and hearing, we examined over 100 species of tree crickets (Oecanthidae), a family with diverse acoustic-related traits that has never been considered in an evolutionary context. We investigated homologous traits related to sound production (stridulatory file, harp, and mirror) and reception (tympana, inner, and outer). Using a robust, time-calibrated molecular phylogeny, we estimated ancestral states and evolutionary rates and tested for correlated evolution. We quantified the phylogenetic signal for each trait to assess how evolutionary relatedness predicted acoustic trait similarity. Our analyses revealed multiple independent losses of sound-producing structures in the forewings and hearing organs, providing evidence for the convergent evolution of the silent phenotype. Our results also suggest a high level of integration among wing veins, particularly those related to acoustic communication. We discuss the potential ecological drivers of these patterns, such as predator avoidance and habitat shifts, and substantiate how alternative phenotypes, like “silent listeners” and “deaf singers”, facilitate evolutionary transitions between acoustic and vibratory signaling (biotremology). Our findings provide a model for understanding the macroevolutionary dynamics of sensory regression, a pattern shared across diverse animal systems. The evolutionary trends in the acoustic signaling of Oecanthidae provide a powerful system for studying the macroevolutionary dynamics of communication.