An ancient genome duplication event drives the development and evolution of spinnerets in spiders.

Abstract

Key appendage innovations have driven the origin and expansion of arthropods, such as spinnerets enabling spiders to occupy three-dimensional space and diversify into more than 53,000 species. Here, we investigate the genetic basis of spinneret emergence in spiders by examining the complex history and functional importance of arachnid genome evolution. Using chromosome-scale genomes from newly sequenced spiders and the whip scorpion, we integrate evidence from macrosynteny and phylogenetic analyses to provide further strong support for a whole-genome duplication (WGD) event that occurred during early Arachnopulmonata evolution. Following this event, the <i>abdominal-A</i> gene pair not only exhibits functional divergence but also jointly facilitates the emergence of spinnerets. Furthermore, we integrated single-cell transcriptomic analyses and functional validation to confirm that the <i>dachshund-1</i> gene also regulates spinneret development. The network of duplicated gene pairs may form a cornerstone in the origin and evolution of key morphological traits, revealing that the long-term effects of ancient WGDs on innovation and diversification also occurred in arthropods.