Rapid molecular diversification and homogenization of clustered major ampullate silk genes in Argiope garden spiders

Abstract

The evolutionary diversification of orb-web weaving spiders is closely tied to the mechanical performance of dragline silk. This proteinaceous fiber provides the primary structural framework of orb web architecture, and its extraordinary toughness allows these structures to absorb the high energy of aerial prey impact. The dominant model of dragline silk molecular structure involves the combined function of two highly repetitive, spider-specific, silk genes (spidroins)—MaSp1 and MaSp2. Recent genomic studies, however, have suggested this framework is overly simplistic, and our understanding of how MaSp genes evolve is limited. Here we present a comprehensive analysis of MaSp structural and evolutionary diversity across species of Argiope (garden spiders). This genomic analysis reveals the largest catalog of MaSp genes found in any spider, driven largely by an expansion of MaSp2 genes. The rapid diversification of Argiope MaSp genes, located primarily in a single genomic cluster, is associated with profound changes in silk gene structure. MaSp2 genes, in particular, have evolved complex hierarchically organized repeat units (ensemble repeats) delineated by novel introns that exhibit remarkable evolutionary dynamics. These repetitive introns have arisen independently within the genus, are highly homogenized within a gene, but diverge rapidly between genes. In some cases, these iterated introns are organized in an alternating structure in which every other intron is nearly identical in sequence. We hypothesize that this intron structure has evolved to facilitate homogenization of the coding sequence. We also find evidence of intergenic gene conversion and identify a more diverse array of stereotypical amino acid repeats than previously recognized. Overall, the extreme diversification found among MaSp genes requires changes in the structure-function model of dragline silk performance that focuses on the differential use and interaction among various MaSp paralogs as well as the impact of ensemble repeat structure and different amino acid motifs on mechanical behavior.

C. elegansepicuticlins define specific compartments in the apical extracellular matrix and function in wound repair

“…Many aECM proteins are composed of imperfect tandem repeats, such elastins (He et al, 2007), gel-forming mucins (Perez-Vilar and Hill, 1999), or silk spidroins (Baker et al, 2022). Epicuticlins are distinctive in containing perfect repeats.…”

Lampshade web spider Ectatosticta davidi chromosome-level genome assembly provides evidence for its phylogenetic position

“…To date, the majority of whole genome-sequenced spiders come from well-studied spider groups such as Araneoidea (Araneidae, Tetragnathidae, Theriidae, Linyphiidae) 19 , 23 , 25 , 28 , 29 , 31 , 32 , 35 – 41 and the marronoid clade (Lycosidae, Pisauridae) 42 . A few genomes have been obtained from Synspermiata (Drymusidae, Dysderidae) 18 and Mygalomorphae (Theraphosidae) 43 (Supplementary Table 1 ).…”

Evolutionary dynamics of glue gene copy number in Drosophila species

“…During animal evolution various glands evolved to produce large amounts of very speci c proteins with diverse functions, such as venom in snakes and frogs or silk in spiders [52,53]. Recent evolutionary studies indicate that, similarly to Drosophila glue genes, the genes encoding these secreted proteins underwent multiple events of gene duplications, losses and conversions in snakes and spiders [54,55]. Our work on Drosophila glue genes, in combination with studies of these other secretory uids, may thus help to provide general insights on how secretory products rapidly adapt to biotic and abiotic factors.…”