Genomic and transcriptomic analyses support a silk gland origin of spider venom glands

Abstract

Background Spiders comprise a hyperdiverse lineage of predators with venom systems, yet the origin of functionally novel spider venom glands remains unclear. Previous studies have hypothesized that spider venom glands originated from salivary glands or evolved from silk-producing glands present in early chelicerates. However, there is insufficient molecular evidence to indicate similarity among them. Here, we provide comparative analyses of genome and transcriptome data from various lineages of spiders and other arthropods to advance our understanding of spider venom gland evolution. Results We generated a chromosome-level genome assembly of a model spider species, the common house spider (Parasteatoda tepidariorum). Module preservation, GO semantic similarity, and differentially upregulated gene similarity analyses demonstrated a lower similarity in gene expressions between the venom glands and salivary glands compared to the silk glands, which questions the validity of the salivary gland origin hypothesis but unexpectedly prefers to support the ancestral silk gland origin hypothesis. The conserved core network in the venom and silk glands was mainly correlated with transcription regulation, protein modification, transport, and signal transduction pathways. At the genetic level, we found that many genes in the venom gland-specific transcription modules show positive selection and upregulated expressions, suggesting that genetic variation plays an important role in the evolution of venom glands. Conclusions This research implies the unique origin and evolutionary path of spider venom glands and provides a basis for understanding the diverse molecular characteristics of venom systems.

Venom gland organogenesis in the common house spider

“…The evolutionary origin of venom glands in spiders remains uncertain and much debated 13,19 . One hypothesis posits that venom glands are modified salivary glands, akin to those of ticks 40,41 .…”

“…Zhu and colleagues 19 advocated the silk gland origin hypothesis based on similarities in the transcriptome profiles of the two organs. However, the absence of key tissues and animal groups in the analysis, such as coxal glands or salivary glands of other arachnid lineages, may have limited consideration of alternative scenarios.…”

“…In addition to the uncertainties surrounding the organogenesis of spider venom glands, their evolutionary origins also remain enigmatic 6 . The current debate revolves around whether the ancestral organs of origin were salivary glands or silk glands 13 , although a recent study found support for the silk gland origin hypothesis based on similarities in the transcriptomes of these two organs 19 .…”

Evolution of the Spider Homeobox Gene Repertoire by Tandem and Whole Genome Duplication

“…We classified the homeobox gene complement of the publicly available chromosome-level genomes from eight spider species, D. silvatica ( Sánchez-Herrero et al 2019 ; Escuer et al 2022 ), D. plantarius ( Blaxter et al 2022 ), L. elegans ( Wang et al 2022 ), P. tepidariorum ( Zhu et al 2023 ), H. graminicola ( Zhu et al 2022 ), A. bruennichi ( Sheffer et al 2021 ), T. antipodiana ( Fan et al 2021 ), and T. clavata ( Hu et al 2022 ). We examined the previous homeobox gene classification of the scorpion C. sculpturatus , which shared the ancestral WGD, as a outgroup to the spiders ( Schwager et al 2017 ; Leite et al 2018 ).…”

Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication

“…We classified the homeobox gene complement of the publicly available chromosomelevel genomes from eight spider species, Dysdera silvatica (Sánchez-Herrero et al 2019;Escuer et al 2022), Dolomedes plantarius (Blaxter et al 2022), Latrodectus elegans (Wang et al 2022), P. tepidariorum (Zhu et al 2023), Hylyphantes graminicola (Zhu et al 2022), Argiope bruennichi (Sheffer et al 2021), Trichonephila antipodiana (Fan et al 2021), and Trichonephila clavata (Hu et al 2022). We examined the previous homeobox gene classification of the scorpion C. sculpturatus, which shared the ancestral WGD, as an outgroup to the spiders (Schwager et al 2017;Leite et al 2018).…”