A role for vocal rhythm in avian speciation

Abstract Bird song mediates speciation but little is known about its genetic basis because of the confounding effect of vocal learning in model systems. Rhythm, in particular, transcends acoustic communication across the animal kingdom and plays a fundamental role in sexual selection and species recognition in birds. Here we investigated the genomic underpinnings of rhythm in vocal non-learning Pogoniulus tinkerbirds using a reference we assembled and 134 further individual whole genomes distributed across a Southern African hybrid zone. We show that rhythm speed is associated with two genes that affect speech in humans, Neurexin-1 and Coenzyme Q8A. Leveraging ancestry, we find that rhythmic stability is also associated with these candidate loci. Furthermore, a pattern of character displacement in rhythmic stability in the contact zone suggests there is reinforcement against hybridization, supported by evidence of assortative mating. Assortative mating is asymmetric, however, occurring only in the species that produces faster, more stable rhythms. Rhythmic stability reflects motor performance, a trait long regarded as an indicator of quality. Because rhythm is an omnipresent trait in animal communication, candidate genes shaping vocal rhythm identified here may play a pivotal role in speciation across birds and other vertebrates.