Diversity and properties of key spider silks and webs
Keywords:
Orbweaver, spider silk, dragline, ecribellate, capture spiralAbstract
Spider silks are natural materials whose diversity surpasses other known silks and man-made polymers. This review covers exciting aspects of the diversity of spider silks and focuses on orb web silks. We argue that to understand silks as biological materials, their functionality must always be considered. The evolution of major ampullate silk provides a good example, as do the properties and functions of the six other silks produced and used by araneid orbweavers. The adhesive snares of the orb webs provide an excellent example of the evolution of two very different forms of silk to capture and hold insect prey, both the wet-glue ecribellate spiders, like the araneids, and the dry-hackled silk of the much older cribellate spiders, like the uloborids. The review concludes by examining how silks may be actively tuned by the spider by adjusting spinning and post-processing conditions. Throughout we argue that this diversity makes spider silks excellent models for polymer research and applications.
References
Agnarsson, I., Kuntner, M. and Blackledge, T. A. 2010. Bioprospecting fi nds the toughest biological material: Extraordinary silk from a giant riverine orb spider. Plos One 5, e11234.
Akai, H., Nagashima, T. and Aoyagi, S. 1993. Ultrastructure of posterior silk gland-cells and liquid silk in indian tasar silkworm, antheraea-mylitta drury (lepidoptera, saturniidae). International Journal of Insect Morphology & Embryology 22, 497-506.
Beek, J. D. v., Kummerlen, J., Vollrath, F. and Meier, B. H. 1999. Supercontracted spider dragline silk: A solid-state nmr study of the local structure. International Journal of Biological Macromolecules 24, 173-178.
Blackledge, T. A. and Hayashi, C. Y. 2006. Silken toolkits: Biomechanics of silk fi bers spun by the orb web spider argiope argentata (fabricius 1775). Journal of Experimental Biology 209, 2452-2461.
Bond, J. E., Garrison, N. L., Hamilton, C. A., Godwin, R. L., Hedin, M. and Agnarsson, I. 2014. Phylogenomics resolves a spider backbone phylogeny and rejects a prevailing paradigm for orb web evolution. Current Biology 24, 1765-1771.
Boutry, C. and Blackledge, T. A. 2010. Evolution of supercontraction in spider silk: Structure-function relationship from tarantulas to orb-weavers. Journal of Experimental Biology 213, 3505-3514.
Boutry, C., Rezac, M. and Blackledge, T. A. 2011. Plasticity in major ampullate silk production in relation to spider phylogeny and ecology. Plos One 6, ee22467.
Brunetta, L. and Craig, C. L. 2010. Spider silk (Ed.) Yale University Press; New Haven.
Bunning, T. J., Jiang, H., Adams, W. W., Crane, R. L., Farmer, B. and Kaplan, D. 1994. Applications of silk. Silk Polymers 544, 353-358.
Cao, Y. and Wang, B. C. 2009. Biodegradation of silk biomaterials. International Journal of Molecular Sciences 10, 1514-1524.
Coddington, J. A. and Levi, H. W. 1991. Systematics and evolution of spiders (araneae). Annual Review of Ecology and Systematics 22, 565-592.
Colgin, M. A. and Lewis, R. V. 1998. Spider minor ampullate silk proteins contain new repetitive sequences and highly conserved non silk-like “Spacer regions”. Protein Science 7, 667-672.
Costa, F. G. and Perez-Miles, F. 1998. Behavior, life cycle and webs of mecicobothrium thorelli (araneae, mygalomorphae, mecicobothriidae). Journal of Arachnology 26, 317-329.
Craig, C. 1997. Evolution of arthropod silks. Annual Review of Entomology 42, 231-267.
Craig, C. L. 1986. Orb-web visibility: The infl uence of insect flight behaviour and visual physiology on the evolution of web designs within the araneoidea. Animal Behaviour 34, 54-68.
Davies, G. J. G., Knight, D. P. and Vollrath, F. 2013. Structure and function of the major ampullate spinning duct of the golden orb weaver, nephila edulis. Tissue & Cell 45, 306-311.
Eberhard, W. G. 1980. Persistant stickiness of cribellum silk. Journal of Arachnology 8, 283.
Eberhard, W. G. 1988. Combing and sticky silk attachment behaviour by cribellate spiders and its taxonomic implications. Bulletin of the British Arachnological Society 7, 247-251.
Edmonds, D. T. and Vollrath, F. 1992. The contribution of atmospheric water vapor to the formation and effi - ciency of a spider’s capture web. Proceedings of the Royal Society of London, Series B: Biological Sciences 248, 145-148.
Fernandez, R., Hormiga, G. and Giribet, G. 2014. Phylogenomic analysis of spiders reveals nonmonophyly of orb weavers. Current Biology 24, 1772-1777.
Fischer, F. and Brander, J. 1960. Eine analyse der gespinste der kreuzspinne. Hoppe-Seylers Zeitschrift Fur Physiologische Chemie 320, 92-102.
Foelix, R. F. 2010. Biology of spiders (Ed. 3rd). Oxford University Press; Oxford, N.Y.
Frische, S., Maunsbach, A. B. and Vollrath, F. 1998. Elongate cavities and skin-core structure in nephila spider silk observed by electron microscopy. Journal of Microscopy-Oxford 189, 64-70.
Frohlich, C. and Buskirk, R. E. 1982. Transmission and attenuation of vibration in orb spider webs. Journal of Theoretical Biology 95, 13-36.
Garb, J. E., DiMauro, T., Lewis, R. V. and Hayashi, C. Y. 2007. Expansion and intragenic homogenization of spider silk genes since the triassic: Evidence from mygalomorphae (tarantulas and their kin) spidroins. Molecular Biology and Evolution 24, 2454-2464.
Gatesy, J., Hayashi, C., Motriuk, D., Woods, J. and Lewis, R. 2001. Extreme diversity, conservation, and convergence of spider silk fi broin sequences. Science 291, 2603-2605.
Gosline, J. M., Guerette, P. A., Ortlepp, C. S. and Savage, K. N. 1999. The mechanical design of spider silks: From fi broin sequence to mechanical function. Journal of Experimental Biology 202, 3295-3303.
Grubb, D. T. and Jelinski, L. W. 1997. Fiber morphology of spider silk: The effects of tensile deformation. Macromolecules 30, 2860-2867.
Guan, J., Porter, D. and Vollrath, F. 2012. Silks cope with stress by tuning their mechanical properties under load. Polymer 53, 2717-2726.
Guan, J., Porter, D. and Vollrath, F. 2013. Thermally induced changes in dynamic mechanical properties of native silks. Biomacromolecules 14, 930-937.
Guan, J., Vollrath, F. and Porter, D. 2011. Two mechanisms for supercontraction in nephila spider dragline silk. Biomacromolecules 12, 4030-4035.
Guerette, P. A., Ginzinger, D. G., Weber, B. H. F. and Gosline, J. M. 1996. Silk properties determined by gland-specifi c expression of a spider fi broin gene family. Science 272, 112-115.
Hayashi, C. Y. 2001. Convergent evolution of sequence elements in spider and insect silk proteins. American Zoologist 41, 1468-1468.
Hayashi, C. Y., Blackledge, T. A. and Lewis, R. V. 2004. Molecular and mechanical characterization of aciniform silk: Uniformity of iterated sequence modules in a novel member of the spider silk fi broin gene family. Molecular Biology and Evolution 21, 1950- 1959.
Hayashi, C. Y., Shipley, N. H. and Lewis, R. V. 1999. Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. International Journal of Biological Macromolecules 24, 271-275.
Hayashi, C. Y., Swanson, B. O., Blackledge, T. A. and Summers, A. P. 2005. Evolution of the material properties of spider dragline silk. Integrative and Comparative Biology 45, 1009-1009.
Hinman, M. B. and Lewis, R. V. 1992. Isolation of a clone encoding a 2nd dragline silk fi broin - nephila-clavipes dragline silk is a 2-protein fi ber. Journal of Biological Chemistry 267, 19320-19324.
Holland, C., Terry, A. E., Porter, D. and Vollrath, F. 2006. Comparing the rheology of native spider and silkworm spinning dope. Nature Materials 5, 870-874.
Holland, C., Vollrath, F., Ryan, A. J. and Mykhaylyk, O. O. 2012. Silk and synthetic polymers: Reconciling 100 degrees of separation. Advanced Materials 24, 105-109.
Klarner, D. and Barth, F. G. 1982. Vibratory signals and prey capture in orb-weaving spiders (zygiella x-notata, nephila clavipes, araneidae). Journal of Comparative Physiology 148, 445-455.
Kluge, J. A., Rabotyagova, O., Leisk, G. G. and Kaplan, D. L. 2008. Spider silks and their applications. Trends in Biotechnology 26, 244-251.
Köhler, T. and Vollrath, F. 1995. Thread biomechanics in the two orb weaving spiders araneus diadematus (araneae, araneidae) and uloborus walckenaerius (araneae, uloboridae). Journal of Experimental Zoology 271, 1-17.
Kopecek, J. and Yang, J. Y. 2007. Revie - hydrogels as smart biomaterials. Polymer International 56, 1078- 1098. Kronenberger, K., Dicko, C. and Vollrath, F. 2012. A novel marine silk. Naturwissenschaften 99, 3-10.
Kronenberger, K. and Vollrath, F. 2015. Spiders spinning electrically charged nano-fi bres. Biology Letters. (in Press).
Kummerlen, J., vanBeek, J. D., Vollrath, F. and Meier, B. H. 1996. Local structure in spider dragline silk investigated by two-dimensional spin-diffusion nuclear magnetic resonance. Macromolecules 29, 2920-2928.
Landolfa, M. A. and Barth, F. G. 1996. Vibrations in the orb web of the spider nephila clavipes: Cues for discrimination and orientation. Journal of Comparative Physiology A: Sensory Neural and Behavioral Physiology 179, 493-508.
Liivak, O., Flores, A., Lewis, R. and Jelinski, L. W. 1997. Conformation of the polyalanine repeats in minor ampullate gland silk of the spider nephila clavipes. Macromolecules 30, 7127-7130.
Lin, L. H., Edmonds, D. T. and Vollrath, F. 1995. Structural engineering of an orb-spider’s web. Nature 373, 146-148.
Liu, Y., Shao, Z. Z. and Vollrath, F. 2005. Relationships between supercontraction and mechanical properties of spider silk. Nature Materials 4, 901-905.
Liu, Y., Sponner, A., Porter, D. and Vollrath, F. 2008. Proline and processing of spider silks. Biomacromolecules 9, 116-121.
Madsen, B., Shao, Z. Z. and Vollrath, F. 1999. Variability in the mechanical properties of spider silks on three levels: Interspecifi c, intraspecifi c and intraindividual. International Journal of Biological Macromolecules 24, 301-306.
Masters, W. M. and Markl, H. 1981. Vibration signal transmission in spider orb webs. Science 213, 363-365.
Mortimer, B., Gordon, S. D., Siviour, C. R., Holland, C., Vollrath, F. and Windmill, J. F. C. 2014. The speed of sound in silk: Linking material performance to biological function. Advanced Materials 26, 5179- 5183.
Mortimer, B., Holland, C. and Vollrath, F. 2013. Forced reeling of bombyx mori silk: Separating behaviour and processing conditions. Biomacromolecules 14, 3653-3659.
Naftilan, S. A. 1999. Transmission of vibrations in funnel and sheet spider webs. International Journal of Biological Macromolecules 24, 289-293.
Opell, B. 1982. Cribellum, calamistrum and ventral comb ontogeny in hyptiotes cavatus (hentz) (araneae: Uloboridae). Bulletin of the British Arachnological Society 5, 338-343.
Opell, B. D. 1993. What forces are responsible for the stickiness of spider cribellar threads. Journal of Experimental Zoology 265, 469-476.
Opell, B. D. 1994a. The ability of spider cribellar prey capture thread to hold insects with different surfacefeatures. Functional Ecology 8, 145-150.
Opell, B. D. 1994b. Factors affecting the diameters of axial fi bers in cribellar threads of the spider family uloboridae. Journal of Arachnology 22, 12-18.
Opell, B. D. 1994c. Factors governing the stickiness of cribellar prey capture threads in the spider family uloboridae. Journal of Morphology 221, 111-119.
Opell, B. D. 1995. Do static electric forces contribute to the stickiness of a spider’s cribellar prey capture threads ? Journal of Experimental Zoology 273, 186- 189.
Ortlepp, C. and Gosline, J. M. 2008. The scaling of safety factor in spider draglines. Journal of Experimental Biology 211, 2832-2840.
Perry, D. J., Bittencourt, D., Siltberg-Liberles, J., Rech, E. L. and Lewis, R. V. 2010. Piriform spider silk sequences reveal unique repetitive elements. Biomacromolecules 11, 3000-3006.
Peters, H. M. 1987. Fine structure and function of capture threads. In: Nentwig, W. (Ed.) Ecophysiology of spiders. Springer, Berlin, pp. 187-202.
Porter, D., Guan, J. and Vollrath, F. 2013. Spider silk: Super material or thin fi bre? Advanced Materials 25, 1275-1279.
Porter, D. and Vollrath, F. 2007. Nanoscale toughness of spider silk. Nano Today 2, 6.
Porter, D. and Vollrath, F. 2009. Silk as a biomimetic ideal for structural polymers. Advanced Materials 21, 487-492.
Riekel, C., Muller, M. and Vollrath, F. 1999. In situ x-ray diffraction during forced silking of spider silk. Macromolecules 32, 4464-4466.
Rousseau, M. E., Lefevre, T. and Pezolet, M. 2009. Conformation and orientation of proteins in various types of silk fi bers produced by nephila clavipes spiders. Biomacromolecules 10, 2945-2953.
Schildknecht, H. 1972. Uber die chemie der spinnwebe, I. Naturwissenschaften 3, 98-99.
Sensenig, A. T., Lorentz, K. A., Kelly, S. P. and Blackledge, T. A. 2012. Spider orb webs rely on radial threads to absorb prey kinetic energy. Journal of the Royal Society Interface 9, 1880-1891.
Shao, Z., Hu, X. W., Frische, S. and Vollrath, F. 1999. Heterogeneous morphology of nephila edulis spider silk and its signifi cance for mechanical properties. Polymer 40, 4709-4711.
Shultz, J. W. 1987. The origin of the spinning apparatus in spiders. Biological Reviews 62, 89-113.
Simmons, A. H., Michal, C. A. and Jelinski, L. W. 1996. Molecular orientation and two-component nature of the crystalline fraction of spider dragline silk. Science 271, 84-87.
Singer, F., Riechert, S. E., Xu, H. F., Morris, A. W., Becker, E., Hale, J. A. and Noureddine, M. A. 2000. Analysis of courtship success in the funnel-web spider agelenopsis aperta. Behaviour 137, 93-117.
Sutherland, T., Young, J. and Weisman, S. 2009. Insect silk: One name, many materials. Annual Review of Entomology 55, 171-188.
Swanson, B. O., Blackledge, T. A. and Hayashi, C. Y. 2007. Spider capture silk: Performance implications of variation in an exceptional biomaterial. Journal of Experimental Zoology 307A, 654-666.
Swanson, B. O., Anderson, S. P., DiGiovine, C., Ross, R. N. and Dorsey, J. P. 2009. The evolution of complex biomaterial performance: The case of spider silk. Integrative and Comparative Biology. p. 21-31.
Szlep, R. 1964. Change in the response of spiders to repeated web vibrations. Behaviour 23, 203-239.
Teule, F., Miao, Y. G., Sohn, B. H., Kim, Y. S., Hull, J. J., Fraser, M. J., Lewis, R. V. and Jarvis, D. L. 2012. Silkworms transformed with chimeric silkworm/ spider silk genes spin composite silk fi bers with improved mechanical properties. Proceedings of the National Academy of Sciences of the United States of America 109, 923-928.
Tian, M. Z., Liu, C. Z. and Lewis, R. 2004. Analysis of major ampullate silk cdnas from two non-orbweaving spiders. Biomacromolecules 5, 657-660.
Tillinghast, E. K. and Sinohara, H. 1984. Carbohydrates associated with the orb web protein of argiope aurantia. Biochemistry International 9, 315-317.
Tillinghast, E. K., Townley, M. A., Bernstein, D. T. and Gallagher, K. S. 1991. Comparative study of orb web hygroscopicity and adhesive spiral composition inthree araneid spiders. Journal of Experimental Zoology 259, 154-165.
Van Nimmen, E., Gellynck, K., Gheysens, T., Van Langenhove, L. and Mertens, J. 2005. Modeling of the stress-strain behavior of egg sac silk of the spider araneus diadematus. Journal of Arachnology 33, 629-639.
Vollrath, F. 1994. General properties of some spider silks. In: Kaplan, D., Wade, W. W., Farmer, B.and Viney, C. (Ed.) Silk polymers: Materials science and biotechnology. American Chemical Society, Washington, pp. 17-28.
Vollrath, F. 1999. Biology of spider silk. International Journal of Biological Macromolecules 24, 81-88.
Vollrath, F. 2006. Spider silk: Thousands of nano-fi laments and dollops of sticky glue. Current Biology 16, R925-R927. Vollrath, F. and Edmonds, D. T. 1989. Modulation of the mechanical-properties of spider silk by coating with water. Nature 340, 305-307.
Vollrath, F., Fairbrother, W. J., Williams, R. J. P., Tillinghast, E. K., Bernstein, D. T., Gallagher, K. S. and Townley, M. A. 1990. Compounds in the droplets of the orb spiders viscid spiral. Nature 345, 526-528.
Vollrath, F. and Knight, D. P. 2001. Liquid crystalline spinning of spider silk. Nature 410, 541-548.
Vollrath, F., Madsen, B. and Shao, Z. Z. 2001. The effect of spinning conditions on the mechanics of a spider’s dragline silk. Proceedings of the Royal Society of London Series B-Biological Sciences 268, 2339- 2346.
Vollrath, F. and Porter, D. 2006. Spider silk as an archetypal protein elastomer. Soft Matter 2, 377-385.
Vollrath, F., Porter, D. and Holland, C. 2011. There are many more lessons still to be learned from spider silks. Soft Matter 7, 9595-9600.
Vollrath, F. and Selden, P. 2007. The role of behavior in the evolution of spiders, silks, and webs. Annual Review of Ecology Evolution and Systematics 38, 819-846.
Vollrath, F. and Tillinghast, E. K. 1991. Glycoprotein glue beneath a spider webs aqueous coat. Naturwissenschaften 78, 557-559.
Wynne, A. 1997. Textiles (Ed.) Macmillan Education; Oxford, UK.
Downloads
Published
Issue
Section
License
This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.
