Decoupling of sexual signals and theirunderlying morphology facilitates rapidphenotypic diversification

How novel phenotypes evolve is challenging to imagine because traits are often underlain by numerous integrated phenotypiccomponents, and changes to any one form can disrupt the function of the entire module. Yet novel phenotypes do emerge, and re-search on adaptive phenotypic evolution suggests that complex traits can diverge while either maintaining existing form–functionrelationships or through innovations that alter form–function relationships. How these alternate routes contribute to sexual signalevolution is poorly understood, despite the role of sexual signals in generating biodiversity. In Hawaiian populations of the Pacificfield cricket, male song attracts both female crickets and a deadly acoustically orienting parasitoid fly. In response to this conflictbetween natural and sexual selection, male crickets have evolved altered wing morphologies multiple times, resulting in loss anddramatic alteration of sexual signals. More recently, we and others have observed a radical increase in sexual signal variation andthe underlying morphological structures that produce song. We conducted the first combined analysis of form (wing morphol-ogy), function (emergent signal), and receiver responses to characterize novel variation, test alternative hypotheses about form–function relationships (Form–Function Continuity vs. Form–Function Decoupling), and investigate underlying mechanistic changesand fitness consequences of novel signals. We identified three sound-producing male morphs (one previously undescribed, named“rattling”) and found that relationships between morphology and signals have been rewired (Form–Function Decoupling), rapidlyand repeatedly, through the gain, loss, and alteration of morphological structures, facilitating the production of signals that existin novel phenotypic space. By integrating across a hierarchy of phenotypes, we uncovered divergent morphs with unique solutionsto the challenge of attracting mates while evading fatal parasitism