Genomic signature of repeated transitions to diurnality in spiders

Repeated transitions to diurnality represent a major behavioral shift in spiders, yet their genomic underpinnings remain largely unknown. Here, we assembled high-quality genomes for nine diurnal spiders using long-read sequencing and compiled diel activity phenotypic data through a combination of systematic literature synthesis and field assessments. By integrating all publicly available spider genomes, we examined the genomic evolutionary dynamics of 67 species including at least 5 independent origins of diurnality. Across diurnal spider lineages, hundreds of genes exhibited convergent shifts in selection, including intensified selection on neural, locomotion, and visual system genes, and relaxed selection on several core phototransduction components. Notably, diurnal spiders showed convergent deceleration in evolutionary rates in circadian regulators, such as CLOCK and CRTC1, and they harbored distinct repertoires of positively selected genes relative to nondiurnal species. In addition, convergent amino acid substitutions were enriched in diurnal hunting spiders. Comparative multitissue transcriptomics showed that genes under convergent selection, particularly those involved in vision, sensory processing, nervous system development, and locomotion, tended to exhibit stronger eye- and central nervous system-biased tissue specificity in diurnal species. Altogether, our results reveal convergent genomic changes associated with repeated evolution of diurnality and illustrate how ecological light environments repeatedly shape the molecular evolution of complex animal behavior.