Sexual selection and predation drive the repeated evolution of stridulation in Heteroptera and other arthropods.

Abstract

Acoustic and substrate-borne vibrations are among the most widely used signalling modalities in animals. Arthropods display a staggering diversity of vibroacoustic organs generating acoustic sound and/or substrate-borne vibrations, and are fundamental to our broader understanding of the evolution of animal signalling. The primary mechanism that arthropods use to generate vibroacoustic signals is stridulation, which involves the rubbing together of opposing body parts. Although stridulation is common, its behavioural context and evolutionary drivers are often hard to pinpoint, owing to limited synthesis of empirical observations on stridulatory species. This is exacerbated by the diversity of mechanisms involved and the sparsity of their description in the literature, which renders their documentation a challenging task. Here, we present the most comprehensive review to date on the systematic distribution and behavioural context of stridulation. We use the megadiverse heteropteran insects as a model, together with multiple arthropod outgroups (arachnids, myriapods, and selected pancrustaceans). We find that stridulatory vibroacoustic signalling has evolved independently at least 84 times and is present in roughly 20% of Heteroptera, representing a remarkable case of convergent evolution. By studying the behavioural context of stridulation across Heteroptera and 189 outgroup lineages, we find that predation pressure and sexual selection are the main behaviours associated with stridulation across arthropods, adding further evidence for their role as drivers of large-scale signalling and morphological innovation in animals. Remarkably, the absence of tympanal ears in most Heteroptera suggests that they typically cannot detect the acoustic component of their stridulatory signals. This demonstrates that the adoption of new signalling modalities is not always correlated with the ability to perceive those signals, especially when these signals are directed towards interspecific receivers in defensive contexts. Furthermore, by mapping their morphology and systematic distribution, we show that stridulatory organs tend to evolve in specific body parts, likely originating from cleaning motions and pre-copulatory displays that are common to most arthropods. By synthesising our understanding of stridulation and stridulatory organs across major arthropod groups, we create the necessary framework for future studies to explore their systematic and behavioural significance, their potential role in sensory evolution and innovation, and the biomechanics of this mode of signalling.