Diverge or merge? Asymmetry in behaviour and genetic introgression at a narrow contact zone and acoustic boundary in learned birdsong

Abstract

Divergence in learned birdsong could act as a pre-mating barrier to reproduction between closely related taxa. Song learning may also lead to heterospecific song copying in contact zones and merging of incipient species. Insight into which of these two evolutionary outcomes is most likely and why may come from behavioral responses to divergent signals. We studied two subspecies of the gray-breasted woodwren (Henicorhina leucophrys leucophrys and H. l. hilaris) that sing distinct songs and replace each other over a narrow contact zone in the Ecuadorian Andes. Combining song analyses, playback experiments and genetic data we explored the role of learned song in driving divergence between these taxa. Our data suggest that song divergence at the contact zone is driven by environmental selection and reinforcement. Behavioral responses to songs were asymmetric; leucophrys responded strongly to both song types while hilaris only responded to songs from their own subspecies. Genetic analysis revealed that introgression was limited to the contact zone and was also asymmetric, with more gene flow from leucophrys to hilaris. Heterospecifc song copying potentially explains this asymmetry: matching genotype to acoustic phenotype showed that hilaris copied leucophrys songs, but not vice-versa. Taken together, we conclude that song learning may promote song divergence and guide assortative mating, but at the same time may allow some genetic introgression between the two taxa at the contact zone. Explaining the presence and direction of asymmetry in genes and behavior at contact zones appears the new challenge and may be critical for understanding ecological speciation.