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

Cultural and genetic variation in animal populations can arise through different mechanisms, often shaped by geographic distance, climatic factors, and habitat connectivity. Patterns of behavioural and genetic diversity may be concordant or discordant, offering an insight into evolutionary and ecological processes. Birds are a good system to explore these dynamics, as their songs are often compared to human languages, reflecting culturally transmitted behavioural traits. While most research has focused mainly on birds with fixed learning repertoires, our study shifts attention to a tropical species with a highly variable and evolving vocal repertoire, offering a closer analogue to human language. To investigate cultural and genetic variation in species with complex songs, we combine fine-scale acoustic, genetic, and behavioural data across a heterogeneous but isolated landscape. We analysed cultural variation from 10,816 songs across 114 individuals using spectral analysis and a linguistic analytical approach of n-grams to evaluate syntax. We tested behavioural responses through 139 playback trials comparing local and non-local songs. Genetic variation was analysed using 10,638 SNPs from 242 sequenced individuals across the species distribution. We find that the fundamental units of songs - notes - carry more information than the spectral features, such as frequency and time. About one-third of note types are shared across individuals across all populations. However, higher levels of song syntax comprised individual-specific patterns but not local dialects. Higher orders of syntax are thus unique to each bird and may be shared only among neighbours. Geographic distance did not predict song similarity. Playback trials further revealed no clear discrimination between local and non-local songs, indicating a recognition that lacks population-level acoustic signatures. In contrast, genetic data reveal an isolation-by-distance pattern with geographic distance significantly explaining genetic population structure. Climatic and habitat heterogeneity, despite being present, did not explain song and genetic variation. Our results demonstrate that cultural and genetic variation can be shaped by distinct processes: genetic variation follows geographic patterns, while song variation reflects highly individualised learning. We highlight the integration of fine-scale acoustic, genetic, and behavioural data to understand how cultural transmission of behavioural traits and genetic population structure exist in a species with a continuously evolving vocal repertoire.