Genomic signatures associated with convergent funnel-web building behavior in spiders

Spiders exhibited diverse and intricate web-building behaviors, which represent a classic model for studying the evolution of complex traits. The funnel-web, a sheet-like web with a retreat tube, has evolved independently in several spider lineages, especially in the families Agelenidae and Macrothelidae. This repeated emergence of a complex behavior offers an example of this funnel-web building behavioral convergence. Here, we present a chromosome-level genome assembly of the agelenid spider Tamgrinia laticeps, along with annotated genomes of another agelenid spider Eratigena atrica, and a macrothelid Orientothele yani which convergently evolved funnel-web building behavior. Comparative genomic analysis of 15 spider species with diverse web-types revealed convergent signatures associated with funnel-web construction. Hundreds of genes tended to experience convergent shift in selective pressure, convergent positive section, and harbored convergent amino acid substitutions. These genes are associated with synaptic transmission (e.g., SLC6A3, Gabbr1, SNAP25), neuromuscular coordination (e.g., ine, VAChT), and behavioral regulation (e.g., Crtc1, Lrrc7). Notably, we detected identical convergent amino acid changes in VAChT and ine across all three funnel-web builders. Our findings demonstrate that convergent evolution of web architecture is linked to nervous system evolution, providing genomic insights into the basis of behavioral convergence.