Behaviour-structure interplay drives acoustic signal divergence: emergence of multiple mechanisms in closely related crickets
Abstract
Acoustic communication is a major driver in reproductive isolation, but the mechanisms underlying signal divergence between closely related species remain unclear. In male crickets, calling song properties result from an interplay between the morphological characteristics of the stridulatory apparatus and the behavioural characteristics controlling forewing movements. The genus Agnothecous, whose morphologically similar species produce high-frequency songs ranging from 10 to 20 kHz, provides an ideal framework for studying this interplay. We analysed 15 species using acoustic recordings, morphological measurements of the stridulatory apparatus, behavioural estimates of forewing kinematics, and comparative phylogenetic methods. Two distinct high-frequency song production mechanisms were identified. Most species use a harmonic amplification model, in which the frequency produced by the stridulatory apparatus generates the fundamental frequency of the song, but the resonant forewings amplify one of its harmonics. In contrast, A. robustus and A. tapinopus have independently evolved towards a high-frequency stridulation model, producing dominant fundamental frequencies directly through accelerated forewing closure. Although they produce similar acoustic results, these mechanisms differ fundamentally in their biomechanics. Phylogenetic analyses indicate that harmonic amplification is ancestral, with high-frequency stridulation having evolved convergently in larger species. Correlation analyses reveal that morphology and behaviour jointly shape acoustic diversity, with body size, forewing kinematics, and the presence of silent intervals in the syllable determining the dominant frequency and temporal parameters of the song. These results highlight the energetic trade-offs and possible irreversibility of high-frequency communication in crickets, illustrating how morphological and behavioural plasticity generate diverse acoustic strategies throughout the evolutionary history of closely related species.