Evolutionary and multi-omic divergences associated with the extreme sexual size dimorphism in spiders

Abstract

Extreme sexual size dimorphism (SSD) represents one of the most striking forms of phenotypic divergence between the sexes, yet the genomic basis of extreme body-size dimorphism remains poorly understood. Orb-weaving spiders exhibit some of the most pronounced female-biased SSD among terrestrial arthropods, providing an exceptional system for investigating the evolutionary and genomic changes associated with extreme SSD. Here, we combined comparative genomics across 51 spider species with sex-resolved transcriptomic and chromatin profiling in the highly dimorphic Joro spider, Trichonephila clavata. Across spiders, we identified SSD-associated evolutionary-rate shifts in genes involved in chromatin regulation, growth, and cuticle structural organization. We further found a significant positive association between JHAMT copy number and SSD, with larger gene repertoires occurring in more extremely dimorphic lineages. In T. clavata, expanded JHAMT paralogs showed sex- and tissue-biased expression together with sex-specific differences in chromatin accessibility and local chromatin interactions. Integrated multi-omic analyses further revealed coordinated sex-specific differences in transcription, chromatin accessibility, and chromatin interactions across genes involved in ecdysteroid signaling, insulin and growth regulation, and epidermal and cuticular processes. Altogether, these findings provide insight into the evolutionary and regulatory changes associated with extreme female-biased SSD in spiders.