How relaxed preferences facilitate the evolution of novel animal signals

The evolution of novel animal signals is critical to the generation of biodiversity. Here, we explore how new sexual signals become established. This process is challenging to explain because if receiver preferences are coupled with existing signals, then most receivers should discriminate against new signals. We investigated an underappreciated hypothesis: relaxed receiver preferences facilitate novel signal evolution by allowing new signals to establish a foothold. Further, we probed the mechanistic underpinnings of relaxed preferences by combining field-based and common garden approaches, allowing us to investigate evolution and plasticity as mechanisms. We capitalized on the Pacific field cricket, Teleogryllus oceanicus, a species that has recently evolved multiple novel acoustic signals (e.g., purring and rattling) in response to an eavesdropping parasitoid fly only found in the crickets' introduced range in Hawaii. To test the hypothesis that selection associated with high search costs in introduced populations leads to relaxed mating preferences and determine whether such relaxation is plastic, we conducted sound preference (phonotaxis) trials with females from the cricket's native range (Australia and French Polynesia, where the fly is absent) and its introduced range (Hawaii, where the fly is present). We presented females with novel songs plus the typical, ancestral song. Differences in phonotactic behavior between the lab and field settings would indicate plasticity in preferences. We found that Australian and French Polynesian females were quite plastic; they discriminated strongly against most songs in the field, but were much more phonotactic to rattling and the typical song in the lab. However, Hawaiian females exhibited little plasticity and were consistently highly responsive to the rattling and typical songs in the lab and field. This pattern points to a loss of ancestral plasticity in female preferences sometime after colonizing Hawaii, resulting in heightened responsiveness to all songs-allowing novel signals to establish.