Rapid sexual signal diversification is facilitated by permissive females

Abstract

The initial process by which novel sexual signals evolve remains unclear, because rare new variants are susceptible to loss by drift or counterselection imposed by prevailing female preferences.^1,2,3,4 We describe the diversification of an acoustic male courtship signal in Hawaiian populations of the field cricket Teleogryllus oceanicus, which was brought about by the evolution of a brachypterous wing morph ("small-wing") only 6 years ago.⁵ Small-wing has a genetic basis and causes silence or reduced-amplitude signaling by miniaturizing male forewings, conferring protection against an eavesdropping parasitoid, Ormia ochracea.⁵ We found that wing reduction notably increases the fundamental frequency of courtship song from an average of 5.1 kHz to 6.4 kHz. It also de-canalizes male song, broadening the range of peak signal frequencies well outside normal song character space. As courtship song prompts female mounting and is sexually selected,^6,7,8,9 we evaluated two scenarios to test the fate of these new signal values. Females might show reduced acceptance of small-wing males, imposing counterselection via prevailing preferences. Alternatively, females might accept small-wing males as readily as long-wing males if their window of preference is sufficiently wide. Our results support the latter. Females preferred males who produced some signal over none, but they mounted sound-producing small-wing males as often as sound-producing long-wing males. Indiscriminate mating can facilitate the persistence of rare, novel signal values. If female permissiveness is a general characteristic of the earliest stages of sexual signal evolution, then taxa with low female mate acceptance thresholds should be more prone to diversification via sexual selection.

Keywords: Telegryllus oceanicus; acoustic signal; evolutionary novelty; host-parasite coevolution; sexual selection; signaler and receiver; wing dimorphism.