Linking genetics, biomechanics, life-history, and behaviour to understand rapid animal signal evolution

Acoustic signals are essential in mate choice and speciation, so understanding factors that promote acoustic divergence will broaden our knowledge of animal signal evolution and the origin of new species. However, signal diversification is expected to be constrained by morphology and biomechanics of sound-producing structures, as well as counter-selection by pre-existing receiver preferences, making early-stage signal diversification extremely rare in nature. In this thesis, I use a rapidly-evolving field cricket, Teleogryllus oceanicus, as a model to investigate how new signal variants emerge and spread. In Hawaii, male mating songs attract both conspecific females and an eavesdropping parasitoid fly, Ormia ochracea, which locates males’ signals and kills them. Under the strong fly selective pressure, acoustic signals of male crickets have been disrupted via genetically-encoded wing polymorphisms, and multiple adaptive male morphs have evolved independently within ca. 20 years (‘flatwing’ and ‘curly-wing’ lost the ability to sing and ‘small-wing’ shifted to different signal values). I investigated the behavioural, bioacoustic, morphological, biomechanical, genetic, genomic, and transcriptomic bases of rapid signal change among these novel morphs. The results firstly indicate how divergent use of alternative mating tactics between these convergent, silent male morphs may enable their co-existence in nature. Next, I characterised the biomechanical basis of rapid sexual signal diversification in small-wing males and determined that it was facilitated by permissive female preferences, which challenges longstanding theory about signal-receiver coevolution. I then tested how these novel signal variants escaped from loss due to drift or counter-selection, finding that the small-wing variant co-opts a pre-existing life-history trade-off that provides additional fitness benefits to both sexes without paying extra costs. As a result, novel signal variants are shielded from extinction. My findings highlight that positive trait covariance involving novel mutations under selection may represent an underappreciated mechanism driving rapid evolution.