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 pre...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-04-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-023-01581-7 |
| _version_ | 1797845763784441856 |
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| author | Bingyue Zhu Pengyu Jin Yiming Zhang Yunxiao Shen Wei Wang Shuqiang Li |
| author_facet | Bingyue Zhu Pengyu Jin Yiming Zhang Yunxiao Shen Wei Wang Shuqiang Li |
| author_sort | Bingyue Zhu |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-09T17:45:18Z |
| format | Article |
| id | doaj.art-b04dabfe70e7492c97030d44ab727cbb |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T17:45:18Z |
| publishDate | 2023-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-b04dabfe70e7492c97030d44ab727cbb2023-04-16T11:25:07ZengBMCBMC Biology1741-70072023-04-0121111710.1186/s12915-023-01581-7Genomic and transcriptomic analyses support a silk gland origin of spider venom glandsBingyue Zhu0Pengyu Jin1Yiming Zhang2Yunxiao Shen3Wei Wang4Shuqiang Li5Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesKey Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of SciencesAbstract 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.https://doi.org/10.1186/s12915-023-01581-7Comparative transcriptomicsGenomicsGene co-expression networksGene selection pressureAdaptive traits |
| spellingShingle | Bingyue Zhu Pengyu Jin Yiming Zhang Yunxiao Shen Wei Wang Shuqiang Li Genomic and transcriptomic analyses support a silk gland origin of spider venom glands BMC Biology Comparative transcriptomics Genomics Gene co-expression networks Gene selection pressure Adaptive traits |
| title | Genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| title_full | Genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| title_fullStr | Genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| title_full_unstemmed | Genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| title_short | Genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| title_sort | genomic and transcriptomic analyses support a silk gland origin of spider venom glands |
| topic | Comparative transcriptomics Genomics Gene co-expression networks Gene selection pressure Adaptive traits |
| url | https://doi.org/10.1186/s12915-023-01581-7 |
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