Microscopic Analyses of the Wasp Spider (Argiope bruennichi) Venom System – Insights into the Architecture
5. Conclusions
Chapter IV
90
favour their stinging apparatus and in centipedes it has recently been established, that their venom evolves under morphological constraints [43, 52].
The wasp spider evolved a rather simple venom composition, likely as a consequence of a mostly silk-based hunting strategy. However, our findings reject the hypothesis that the architecture of its venom apparatus differs from those described from other previously studied. Reflecting the typical morphology for araneomorphs, it is composed of labidognathous chelicerae that appear functionally and shape-wise comparable to spiders with a similar body size. Moreover, the associated venom gland is rather large and reaches deep into the prosoma, indicating that this system yields large quantities of venom for a small araneomorph spider. The muscular layers that cover the venom gland as well as the attached nerves mirror the structure present in spiders from other families. The overall structure of the venom gland equally resembles that of other spiders. In all species so far studied, the venom gland comprises a complex network of secretory cells, granules, vesicles and cytoplasmic projections albeit minor structural differences occur.
Chapter IV
91
[1] V. Schendel, L. D. Rash, R. A. Jenner, and E. A. B. Undheim, “The diversity of venom: The importance of behavior and venom system morphology in understanding its ecology and evolution,” Toxins. 2019, doi:
10.3390/toxins11110666.
[2] B. G. Fry et al., “The Toxicogenomic Multiverse: Convergent Recruitment of Proteins Into Animal Venoms,” Annu.
Rev. Genomics Hum. Genet., 2009, doi: 10.1146/annurev.genom.9.081307.164356.
[3] N. R. Casewell, W. Wüster, F. J. Vonk, R. A. Harrison, and B. G. Fry, “Complex cocktails: The evolutionary novelty of venoms,” Trends in Ecology and Evolution. 2013, doi: 10.1016/j.tree.2012.10.020.
[4] World Spider Catalog, “World Spider Catalog Version 20.5.,” Nat. Hist. Museum Bern, 2019, doi: 10.24436/2.
[5] N. J. Saez et al., “Spider-venom peptides as therapeutics,” Toxins. 2010, doi: 10.3390/toxins2122851.
[6] N. Langenegger, W. Nentwig, and L. Kuhn-Nentwig, “Spider venom: Components, modes of action, and novel strategies in transcriptomic and proteomic analyses,” Toxins. 2019, doi: 10.3390/toxins11100611.
[7] N. J. Saez and V. Herzig, “Versatile spider venom peptides and their medical and agricultural applications,”
Toxicon, 2019, doi: 10.1016/j.toxicon.2018.11.298.
[8] K. L. Richards et al., “Selective NaV1.1 activation rescues Dravet syndrome mice from seizures and premature death,” Proc. Natl. Acad. Sci. U. S. A., 2018, doi: 10.1073/pnas.1804764115.
[9] G. F. King and M. C. Hardy, “Spider-Venom Peptides: Structure, Pharmacology, and Potential for Control of Insect Pests,” Annu. Rev. Entomol., 2013, doi: 10.1146/annurev-ento-120811-153650.
[10] I. R. Chassagnon et al., “Potent neuroprotection after stroke afforded by a double-knot spider-venom peptide that inhibits acid-sensing ion channel 1a,” Proc. Natl. Acad. Sci. U. S. A., 2017, doi: 10.1073/pnas.1614728114.
[11] V. Herzig, G. F. King, and E. A. B. Undheim, “Can we resolve the taxonomic bias in spider venom research?,”
Toxicon X, 2019, doi: 10.1016/j.toxcx.2018.100005.
[12] T. Lüddecke, A. Vilcinskas, and S. Lemke, “Phylogeny-guided selection of priority groups for venom bioprospecting: Harvesting toxin sequences in tarantulas as a case study,” Toxins (Basel)., vol. 11, no. 9, 2019, doi:
10.3390/toxins11090488.
[13] V. L. P. Dos Santos et al., “Structural and ultrastructural description of the venom gland of Loxosceles intermedia (brown spider),” Toxicon, 2000, doi: 10.1016/S0041-0101(99)00155-5.
[14] L. M. Silva et al., “Structural analysis of the venom glands of the armed spider Phoneutria nigriventer (Keyserling, 1891): Microanatomy, fine structure and confocal observations,” Toxicon, 2008, doi: 10.1016/j.toxicon.2007.12.009.
[15] E. V. Grishin, “Black widow spider toxins: The present and the future,” in Toxicon, 1998, doi: 10.1016/S0041-0101(98)00162-7.
[16] J. E. Garb, “Extraction of venom and venom gland microdissections from spiders for proteomic and transcriptomic analyses,” J. Vis. Exp., 2014, doi: 10.3791/51618.
[17] U. Järlfors, D. S. Smith, and F. E. Russell, “Nerve endings in the venom gland of the spider Latrodectus mactans,”
Toxicon, 1969, doi: 10.1016/0041-0101(69)90025-7.
[18] D. S. Smith and F. E. Russel, “Structure of the venom gland of the black widow spider Latrodectus mactans. A preliminary light and electron microscopic study” in Animal Toxins, 1967.
[19] J. Kovoor and A. Muñoz-Cuevas, “Comparative histology of the venom glands in a lycosid and several oxyopid spiders (Araneae),” Ekologia Bratislava. 2000.
[20] N. Yigit, A. Bayram, T. Danisman, Z. Sancak, and M. G. Tel, “Morphological characterization of the venom apparatus in the wolf spider Lycosa singoriensis (Laxmann, 1770),” J. Venom. Anim. Toxins Incl. Trop. Dis., 2009, doi:
10.1590/S1678-91992009000100013.
[21] K. Çavuşoǧlu, A. Bayram, M. Maraş, T. Kirindi, and K. Çavuşoǧlu, “A morphological study on the venom apparatus of spider Larinioides cornustus (Araneae, Araneidae),” Turkish J. Zool., 2005.
[22] N. Yiǧit, A. Bayram, T. Danişman, and Z. Sancak, “Functional morphology of the venom apparatus of Larinioides ixobolus (Araneae: Araneidae),” Pakistan J. Biol. Sci., 2006, doi: 10.3923/pjbs.2006.1975.1978.
[23] T. A. A. Rocha-e-Silva, C. B. Collares-Buzato, M. A. da Cruz-Höfling, and S. Hyslop, “Venom apparatus of the brazilian tarantula Vitalius dubius Mello-Leitão 1923 (Theraphosidae),” Cell Tissue Res., 2009, doi: 10.1007/s00441-008-0738-x.
[24] M. Benli, M. Karakas, N. Yigit, and S. Cebesoy, “Determining with SEM, structure of the venom apparatus in the tube web spider, Segestria florentina (Araneae: Segestriidae),” J. Entomol. Zool. Stud., 2013.
[25] S. Malt, F. W. Sander, and G. Schaller, “Contribution to foraging ecology of selected Araneidae in xerophil grasslands with particular consideration of Argiope brunnichii Scop.,” Zool. Jahrbucher Abteilung fur Systenatik, Okol.
und Geogr. der Tiere, 1990.
[26] D. G. E. Gomes, “Orb-weaving spiders are fewer but larger and catch more prey in lit bridge panels from a natural artificial light experiment,” PeerJ, 2020, doi: 10.7717/peerj.8808.
[27] R. E. Buskirk, “Coloniality, Activity Patterns and Feeding in a Tropical Orb-Weaving Spider,” Ecology, 1975, doi:
10.2307/1934699.
[28] A. M. Heiling, “Why do nocturnal orb-web spiders (Araneidae) search for light?,” Behav. Ecol. Sociobiol., 1999, doi:
10.1007/s002650050590.
Chapter IV
92
[29] J. M. Biere and G. W. Uetz, “Web Orientation in the Spider Micrathena Gracilis (Araneae: Araneidae),” Ecology, 1981, doi: 10.2307/1936708.
[30] K. W. Welke and J. M. Schneider, “Sexual cannibalism benefits offspring survival,” Anim. Behav., 2012, doi:
10.1016/j.anbehav.2011.10.027.
[31] M. Nyffeler and G. Benz, “Foraging ecology and predatory importance of a guild of orb-weaving spiders in a grassland habitat,” J. Appl. Entomol., 1989, doi: 10.1111/j.1439-0418.1989.tb00246.x.
[32] T. Eisner and J. Dean, “Ploy and counterploy in predator - prey interactions: orb weaving spiders versus bombardier beetles,” Proc. Natl. Acad. Sci. U. S. A., 1976, doi: 10.1073/pnas.73.4.1365.
[33] R. Václav and P. Prokop, “Does the appearance of orbweaving spiders attract prey?,” Ann. Zool. Fennici, 2006.
[34] L. Fromhage, G. Uhl, and J. M. Schneider, “Fitness consequences of sexual cannibalism in female Argiope bruennichi,” Behav. Ecol. Sociobiol., 2003, doi: 10.1007/s00265-003-0656-6.
[35] S. P. Chinta, S. Goller, J. Lux, S. Funke, G. Uhl, and S. Schulz, “The sex pheromone of the wasp spider Argiope bruennichi,” Angew. Chemie - Int. Ed., 2010, doi: 10.1002/anie.200906311.
[36] A. Walter, P. Bliss, M. A. Elgar, and R. F. A. Moritz, “Argiope bruennichi shows a drinking-like behaviour in web hub decorations (Araneae, Araneidae),” J. Ethol., 2009, doi: 10.1007/s10164-007-0077-5.
[37] H. Krehenwinkel, D. Rödder, and D. Tautz, “Eco-genomic analysis of the poleward range expansion of the wasp spider Argiope bruennichi shows rapid adaptation and genomic admixture,” Glob. Chang. Biol., 2015, doi:
10.1111/gcb.13042.
[38] H. Krehenwinkel and D. Tautz, “Northern range expansion of European populations of the wasp spider Argiope bruennichi is associated with global warming-correlated genetic admixture and population-specific temperature adaptations,” Mol. Ecol., 2013, doi: 10.1111/mec.12223.
[39] S. M. Zimmer, H. Krehenwinkel, and J. M. Schneider, “Rapid range expansion is not restricted by inbreeding in a sexually cannibalistic spider,” PLoS One, 2014, doi: 10.1371/journal.pone.0095963.
[40] W. Wawer, R. Rutkowski, H. Krehenwinkel, D. Lutyk, K. Pusz-Bocheńska, and W. Bogdanowicz, “ Population structure of the expansive wasp spider ( Argiope bruennichi ) at the edge of its range ,” J. Arachnol., 2017, doi:
10.1636/joa-s-16-056.1.
[41] T. Lüddecke et al., “An Economic Dilemma Between Molecular Weapon Systems May Explain an Arachnological-atypical Venom in Wasp Spiders (Argiope bruennichi),” Biomolecules, vol. 10, no. 7, p. 978, 2020.
[42] Z. Duan, R. Cao, L. Jiang, and S. Liang, “A combined de novo protein sequencing and cDNA library approach to the venomic analysis of Chinese spider Araneus ventricosus,” J. Proteomics, 2013, doi: 10.1016/j.jprot.2012.10.011.
[43] E. A. B. Undheim et al., “Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint,” Proc. Natl. Acad. Sci. U. S. A., 2015, doi: 10.1073/pnas.1424068112.
[44] R. F. Foelix, “Biology of Spiders,” Insect Syst. Evol., 1983, doi: 10.1163/187631283X00371.
[45] S. L. Zonstein, “The spider chelicerae: some problems of origin evolution,” Proc. 21st Eur. Colloq. Arachnol., 2003.
[46] L. Kuhn-Nentwig, R. Stöcklin, and W. Nentwig, “Venom composition and strategies in spiders. is everything possible?,” in Advances in Insect Physiology, 2011.
[47] M. J. Moon and M. H. Yu, “Fine structure of the chelicera in the spider Nephila clavata,” Entomol. Res., 2007, doi:
10.1111/j.1748-5967.2007.00108.x.
[48] H. Hu, P. K. Bandyopadhyay, B. M. Olivera, and M. Yandell, “Characterization of the Conus bullatus genome and its venom-duct transcriptome,” BMC Genomics, 2011, doi: 10.1186/1471-2164-12-60.
[49] R. H. Valente et al., “The primary duct of Bothrops jararaca glandular apparatus secretes toxins,” Toxins (Basel)., 2018, doi: 10.3390/toxins10030121.
[50] L. L. Tayo, B. Lu, L. J. Cruz, and J. R. Yates, “Proteomic analysis provides insights on venom processing in Conus textile,” J. Proteome Res., 2010, doi: 10.1021/pr901032r.
[51] M. Li, B.G. Fry, R.M. Kini, "Eggs-only diet: its implications for the toxin rofile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J Mol Evol, 2005, 60(1): 81-89.
[52] G.S. Casper, "Prey capture and stinging behaviour in the Emporer Scorpion, Pandinus imperator (Koch) (Scorpiones, Scorpionidae). J Arachnol 1985, 13(3): 277-283.
93