The Complex Interplay between Evolutionary Flexibility and Diversification in a Family of Spiders

Understanding the mechanisms of how morphological traits drive speciation and contribute to species richness is pivotal in evolutionary biology. In this context, the evolutionary flexibility of morphological traits may play a significant role. Using the diverse daddy long-legs spiders, Pholcidae, which currently includes some 2,000 described species, we explored the interplay between speciation rate, trait evolution rate, microhabitat shift rate, species richness, interspecific variability of body size, leg length, relative leg length, and leg proportions. We applied a combination of large-scale genomic and taxonomic sampling, and phylogenetic and comparative analyses to assess the dynamics of diversification and evolutionary flexibility (measured as either the standard variance or disparity of traits), as well as their interactions. We found that increased evolutionary flexibility is accompanied with accelerated rates in speciation and trait evolution, and with higher species richness. We also observed near-isometry of leg length and body size in the species-rich lineages, suggesting stabilizing selection, while positive allometry in the species-poor lineages indicates directional selection. Additionally, we found a positive correlation between trait evolution rates and microhabitat shifts. We argue that environmental heterogeneity and frequent microhabitat shifts may contribute to the origin and maintenance of evolutionary flexibility, which in turn influences the organisms' ability to exploit new resources and habitats. On the other hand, our study suggests that a lack of evolutionary flexibility, e.g. due to dwarfism or gigantism, could be an evolutionary dead end. This study enhances our understanding of the mechanisms of diversification, demonstrating that evolutionary flexibility of morphological traits may vary among closely related taxa and is likely to have contributed to the uneven distribution of biodiversity across the tree of life.