Distinct, asynchronous processes underlie cultural and genetic variation in a bird species with complex song repertoires

Dialects in birdsongs represent population clusters and cultural diversity. Cultural and genetic variation in animals, however, do not always evolve along the same trajectory. Few studies have tested this in a wild songbird with a continuous learning strategy. Songbirds (oscine Passeriformes) with a continual learning window exhibit great song diversity and may show cultural differentiation that outpaces genetic divergence. We investigate cultural and genetic variation in a tropical endemic songbird in a topographically and climatically complex sky-island landscape of the Western Ghats of India. We combine fine-scale acoustic, behavioural, and genetic data: from 90 individuals (10,816 songs), analysed using frequency-temporal parameters and a linguistic method for syntax; a playback experiment with 136 trials to compare behavioural responses to local and non-local songs; and blood samples from 242 individuals (10,638 SNPs) to infer genetic population structure. We find no difference in songs across locations and individuals in the time-frequency domain, but only in syntax. One-third of notes, the smallest vocal units, are widely shared across all individuals in their distribution. Longer note combinations result in greater individual differences within populations, but only form small differences between populations. Geographic distance strongly predicts genetic but not song syntactic differences, and playback experiments show equal responses to local and non-local songs. Thus, strong individual signatures but weak local-level dialects are generated by a shared note repertoire and associated combinatorial syntax. We highlight that cultural transmission may operate at fine social scales, decoupled from genetic structure, which is strongly driven by isolation-by-distance. Significance statement Whether learned behaviours exhibit patterns similar to those of inherited genes remains a long-standing question in evolutionary biology. Birdsong has a strong cultural component paralleling human language, yet most knowledge comes from birds with a narrow learning window. Open-ended learners, who acquire new songs throughout life like humans, are poorly documented in the wild. We studied such a songbird restricted to the tropical cloud montane forests of southern India. Songs appear acoustically similar across populations but differ in how basic units are ordered (syntax), while individuals are more distinct from each other in longer note combinations than populations are. Genetic similarity decreased with geographic distance. Culturally learned traits can thus evolve independently of genetic structure, showing how learning decouples behaviour from geography-driven genetic ancestry.