The rise and diversification of spidroins in the deep-time evolution of spiders

The evolutionary success of spiders is often attributed to their stunning ability to produce and utilize silk, but the potential link between the molecular and phenotypic basis of silk production and spider diversification is seldom tested in a robust dated phylogenetic framework. Here, we provide a macroevolutionary context for testing hypotheses by reconstructing and dating the spider tree of life using genomic and transcriptomic data. We searched exhaustively for members of the spider silk protein (spidroin) gene family from omics data and identified them in an iterative phylogenetic pipeline. Four distinct new types of spidroins with atypical sequence characteristics are discovered to be widespread in true spiders with the potential to affect silk properties, as inferred by our phylogenetic generalized linear mixed model and phylogenetic generalized least squares analyses. Combining our robust dated phylogenomic tree of spiders and a comprehensive spidroin dataset, a comprehensive picture of spidroin evolution is revealed. By performing state speciation and extinction analyses, we discovered that only the presence of aggregate gland is linked to a higher diversification rate among all binary spidroin-related characters, while the speciation rate of spiders is dependent on the number of ampullate-gland-associated-atypical spidroin types, silk gland types, total spidroin copies, and total spidroin types.