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

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.

A trade-off in evolution: the adaptive landscape of spiders without venom glands.

BACKGROUND: Venom glands play a key role in the predation and defense strategies of almost all spider groups. However, the spider family Uloboridae lacks venom glands and has evolved an adaptive strategy: they excessively wrap their prey directly with spider silk instead of paralyzing it first with toxins. This shift in survival strategy is very fascinating, but the genetic underpinnings behind it are poorly understood. RESULTS: Spanning multiple spider groups, we conducted multiomics analyses on Octonoba sinensis and described the adaptive evolution of the Uloboridae family at the genome level. We observed the coding genes of myosin and twitchin in muscles are under positive selection, energy metabolism functions are enhanced, and gene families related to tracheal development and tissue mechanical strength are expanded or emerged, all of which are related to the unique anatomical structure and predatory behavior of spiders in the family Uloboridae. In addition, we also scanned the elements that are absent or under relaxed purifying selection, as well as toxin gene homologs in the genomes of 2 species in this family. The results show that the absence of regions and regions under relaxed selection in these spiders' genomes are concentrated in areas related to development and neurosystem. The search for toxin homologs reveals possible gene function shift between toxins and nontoxins and confirms that there are no reliable toxin genes in the genome of this group. CONCLUSIONS: This study demonstrates the trade-off between different predation strategies in spiders, using either chemical or physical strategy, and provides insights into the possible mechanism underlying this trade-off. Venomless spiders need to mobilize multiple developmental and metabolic pathways related to motor function and limb mechanical strength to cover the decline in adaptability caused by the absence of venom glands.

Single-cell transcriptomics reveals the brain evolution of web-building spiders.

Spiders are renowned for their efficient capture of flying insects using intricate aerial webs. How the spider nervous systems evolved to cope with this specialized hunting strategy and various environmental clues in an aerial space remains unknown. Here we report a brain-cell atlas of >30,000 single-cell transcriptomes from a web-building spider (Hylyphantes graminicola). Our analysis revealed the preservation of ancestral neuron types in spiders, including the potential coexistence of noradrenergic and octopaminergic neurons, and many peptidergic neuronal types that are lost in insects. By comparing the genome of two newly sequenced plesiomorphic burrowing spiders with three aerial web-building spiders, we found that the positively selected genes in the ancestral branch of web-building spiders were preferentially expressed (42%) in the brain, especially in the three mushroom body-like neuronal types. By gene enrichment analysis and RNAi experiments, these genes were suggested to be involved in the learning and memory pathway and may influence the spiders' web-building and hunting behaviour. Our results provide key sources for understanding the evolution of behaviour in spiders and reveal how molecular evolution drives neuron innovation and the diversification of associated complex behaviours.