Cis-regulatory divergence and mate recognition in behaviourally isolated cricket species

Cis-regulatory evolution has been implicated in morphological and physiological reproductive isolation, but its role in divergence of mate recognition behaviours is unknown. The latter are often the first, most powerful mating barriers to evolve during speciation, but understanding their genetics is hampered by the context-dependence of mate choice. We circumvented this challenge by using allele-specific expression analyses in F ₁ hybrids of sexually isolated cricket species, Teleogryllus oceanicus and T. commodus . Female crickets choose mating partners based on species-specific male advertisement songs, and we found extensive cis-regulatory divergence in neural tissues exposed to conspecific, heterospecific, or mixed-species songs. Genes with divergent expression were implicated in learning, memory and transcriptional regulation, and they showed elevated population genetic differentiation in allopatry but not sympatry. This implies that genes recruited during evolutionary divergence of mate recognition systems may be homogenised by gene flow. Regulatory divergence was asymmetrical between the two species; divergent selection on genes associated with female perception of male song was more prominent in T. oceanicus than in T. commodus . Evolved differences in gene regulation are strongly associated with sexual signal perception in closely related species, supporting the idea that rapid cis-regulatory evolution of mate recognition can accelerate speciation.