The Science of Nature

, 104:67 | Cite as

Punctuated evolution of viscid silk in spider orb webs supported by mechanical behavior of wet cribellate silk

  • Dakota Piorkowski
  • Todd A. BlackledgeEmail author
Original Paper


The origin of viscid capture silk in orb webs, from cribellate silk-spinning ancestors, is a key innovation correlated with significant diversification of web-building spiders. Ancestral cribellate silk consists of dry nanofibrils surrounding a stiff, axial fiber that adheres to prey through van der Waals interactions, capillary forces, and physical entanglement. In contrast, viscid silk uses chemically adhesive aqueous glue coated onto a highly compliant and extensible flagelliform core silk. The extensibility of the flagelliform fiber accounts for half of the total work of adhesion for viscid silk and is enabled by water in the aqueous coating. Recent cDNA libraries revealed the expression of flagelliform silk proteins in cribellate orb-weaving spiders. We hypothesized that the presence of flagelliform proteins in cribellate silk could have allowed for a gradual shift in mechanical performance of cribellate axial silk, whose effect was masked by the dry nature of its adhesive. We measured supercontraction and mechanical performance of cribellate axial silk, in wet and dry states, for two species of cribellate orb web-weaving spiders to see if water enabled flagelliform silk-like performance. We found that compliance and extensibility of wet cribellate silk increased compared to dry state as expected. However, when compared to other silk types, the response to water was more similar to other web silks, like major and minor ampullate silk, than to viscid silk. These findings support the punctuated evolution of viscid silk mechanical performance.


Biomaterial Spider Silk Cribellate Orb web Tensile properties 



We thank Lance Johnson for assistance collecting silk samples, Matjaž Gregorič for collecting U. plumipes spiders, and Chen-Pan Liao for assistance with statistical analysis. This work was funded by the National Science Foundation.


  1. Amarpuri G, Zhang C, Diaz C, Opell BD, Blackledge TA, Dhinojwala A (2015) Spiders tune glue viscosity to maximize adhesion. ACS Nano 9(11):11472–11478CrossRefPubMedGoogle Scholar
  2. Blackledge TA, Hayashi CY (2006a) Unraveling the mechanical properties of composite silk threads spun by cribellate orb-weaving spiders. J Exper Biol 209:3131–3140CrossRefGoogle Scholar
  3. Blackledge TA, Hayashi CY (2006b) Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775). J Exper Biol 209(13):2452–2461CrossRefGoogle Scholar
  4. Blackledge TA, Cardullo RA, Hayashi CY (2005) Polarized light microscopy, variability in spider silk diameters and the mechanical characterization of spider silk. Invert Biol 124(2):165–173CrossRefGoogle Scholar
  5. Blackledge TA, Scharff N, Coddington JA, Szüts T, Wenzel JW, Hayashi CY, Agnarsson I (2009a) Reconstructing web evolution and spider diversification in the molecular era. Proc National Acad Sci 106(13):5229–5234CrossRefGoogle Scholar
  6. Blackledge TA, Boutry C, Wong SC, Baji A, Dhinojwala A, Sahni V, Agnarsson I (2009b) How super is supercontraction? Persistent versus cyclic responses to humidity in spider dragline silk. J Exper Biol 212(13):1981–1989CrossRefGoogle Scholar
  7. Blackledge TA, Kuntner M, Agnarsson I (2011) The form and function of spider orb webs: evolution from silk to ecosystems. Adv Insect Phys 41:175CrossRefGoogle Scholar
  8. Bond JE, Opell BD (1998) Testing adaptive radiation and key innovation hypotheses in spiders. Evolution:403–414Google Scholar
  9. Bond JE, Garrison NL, Hamilton CA, Godwin RL, Hedin M, Agnarsson I (2014) Phylogenomics resolves a spider backbone phylogeny and rejects a prevailing paradigm for orb web evolution. Curr Biol 24:1765–1771CrossRefPubMedGoogle Scholar
  10. Bott RA, Baumgartner W, Bräunig P, Menzel F, Joel AC (2017) Adhesion enhancement of cribellate capture threads by epicuticular waxes of the insect prey sheds new light on spider web evolution. Proc R Soc B 284(1855):20170363CrossRefPubMedGoogle Scholar
  11. Boutry C, Blackledge TA (2010) Evolution of supercontraction in spider silk: structure-function relationship from tarantulas to orb-weavers. J Exper Biol 213(20):3505–3514CrossRefGoogle Scholar
  12. Boutry C, Řezáč M, Blackledge TA (2011) Plasticity in major ampullate silk production in relation to spider phylogeny and ecology. PLoS One 6(7):e22467CrossRefPubMedPubMedCentralGoogle Scholar
  13. Coddington JA (1982) Monophyletic origin of orb-webs. Amer Zool 22(4):886–886Google Scholar
  14. Coddington JA (1986) The monophyletic origin of the orb web. In: Shear WA (ed) spiders: webs, behavior, and evolution, 319-63. Stanford University Press, StanfordGoogle Scholar
  15. Coddington JA (1990) Cladistics and spider classification: araneomorph phylogeny and the monophyly of orbweavers (Araneae: Araneomorphae; Orbiculariae). Acta Zool Fenn 190(190):75–87Google Scholar
  16. Coddington JA, Levi HW. (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst (1):565–92Google Scholar
  17. Colgin MA, Lewis RV (1998) Spider minor ampullate silk proteins contain new repetitive sequences and highly conserved non-silk-like “spacer regions”. Protein Sci 7(3):667–672CrossRefPubMedPubMedCentralGoogle Scholar
  18. Creager MS, Jenkins JE, Thagard-Yeaman LA, Brooks AE, Jones JA, Lewis RV, Holland GP, Yarger JL (2010) Solid-state NMR comparison of various spiders’ dragline silk fiber. Biomacromolecules 11(8):2039CrossRefPubMedPubMedCentralGoogle Scholar
  19. Denny M (1976) The physical properties of spider’s silk and their role in the design of orb-webs. J Exper Biol 65(2):483–506Google Scholar
  20. Dimitrov D, Lopardo L, Giribet G, Arnedo MA, Álvarez-Padilla F, Hormiga G (2011) Tangled in a sparse spider web: single origin of orb weavers and their spinning work unravelled by denser taxonomic sampling. Proc R Soc B 279:1341–1350CrossRefPubMedPubMedCentralGoogle Scholar
  21. Eberhard WG (1982) Behavioral characters for the higher classification of orb-weaving spiders. Evolution 1067–95Google Scholar
  22. Eberhard WG (1990) Function and phylogeny of spider webs. Annu Rev Ecol Syst 21(1):341–372CrossRefGoogle Scholar
  23. Eberhard WG, Barrantes G (2015) Cues guiding uloborid construction behavior support orb web monophyly. J Arachnol 43(3):371–387CrossRefGoogle Scholar
  24. Eles PT, Michal CA (2004) Strain dependent local phase transitions observed during controlled supercontraction reveal mechanisms in spider silk. Macromolecules 37(4):1342–1345CrossRefGoogle Scholar
  25. Elettro H, Neukirch S, Antkowiak A, Vollrath F (2015) Adhesion of dry and wet electrostatic capture silk of uloborid spider. Sci Nat (7–8):1–4Google Scholar
  26. Fernandez R, Hormiga G, Giribet G (2014) Phylogenomic analysis of spiders reveals nonmonophyly of orb weavers. Curr Biol 24:1772–1777CrossRefPubMedGoogle Scholar
  27. Foelix R (2011) Biology of spiders, 3rd edn. Oxford Univ. Press, OxfordGoogle Scholar
  28. Garb JE, DiMauro T, Vo V, Hayashi CY (2006) Silk genes support the single origin of orb webs. Science 312(5781):1762CrossRefPubMedGoogle Scholar
  29. Garrison NL, Rodriguez J, Agnarsson I, Coddington JA, Griswold CE, Hamilton CA, Hedin M, Kocot KM, Ledford JM, Bond JE (2016) Spider phylogenomics: untangling the Spider Tree of Life. PeerJ 4:e1719CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gatesy J, Hayashi C, Motriuk D, Woods J, Lewis R (2001) Extreme diversity, conservation, and convergence of spider silk fibroin sequences. Science 291(5513):2603–2605CrossRefPubMedGoogle Scholar
  31. Gosline JM, Denny MV, Demont ME (1984) Spider silk as rubber. Nature 309:551–552CrossRefGoogle Scholar
  32. Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8(1):4–15CrossRefGoogle Scholar
  33. Griswold CE, Coddington JA, Platnick NI, Forster RR (1999) Towards a phylogeny of entelegyne spiders (Araneae, Araneomorphae, Entelegynae). J Arachnol 53–63Google Scholar
  34. Griswold CE, Ramírez MJ, Coddington JA, Platnick NI (2005) Atlas of phylogenetic data for entelegyne spiders (Araneae: araneomorphae: Entelegynae), with comments on their phylogeny. Proc Cal Acad Sci 56:1–324Google Scholar
  35. Guinea GV, Pérez-Rigueiro J, Plaza GR, Elices M (2006) Volume constancy during stretching of spider silk. Biomacromolecules 7(7):2173–2177CrossRefPubMedGoogle Scholar
  36. Guinea GV, Cerdeira M, Plaza GR, Elices M, Pérez-Rigueiro J (2010) Recovery in viscid line fibers. Biomacromolecules 11(5):1174–1179CrossRefPubMedGoogle Scholar
  37. Guinea GV, Elices M, Plaza GR, Perea GB, Daza R, Riekel C, Agulló-Rueda F, Hayashi C, Zhao Y, Perez-Rigueiro J (2012) Minor ampullate silks from Nephila and Argiope spiders: tensile properties and microstructural characterization. Biomacromolecules 13(7):2087–2098CrossRefPubMedGoogle Scholar
  38. Hawthorn AC, Opell BD (2002) Evolution of adhesive mechanisms, in cribellar spider prey capture thread: evidence for van der Waals and hygroscopic forces. Biol J Linn Soc Lond 77:1–8CrossRefGoogle Scholar
  39. Hawthorn AC, Opell BD (2003) van der Waals and hygroscopic forces of adhesion generated by spider capture threads. J Exper Biol 206:3905–3911CrossRefGoogle Scholar
  40. Hayashi CY, Lewis RV (1998) Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. J Mol Biol 275(5):773–784CrossRefPubMedGoogle Scholar
  41. Hayashi CY, Lewis RV (2000) Molecular architecture and evolution of a modular spider silk protein gene. Science 287(5457):1477–1479CrossRefPubMedGoogle Scholar
  42. Hayashi CY, Blackledge TA, Lewis RV (2004) Molecular and mechanical characterization of aciniform silk: uniformity of iterated sequence modules in a novel member of the spider silk fibroin gene family. Mol Biol Evol 21(10):1950–1959CrossRefPubMedGoogle Scholar
  43. Jelinski LW (1998) Establishing the relationship between structure and mechanical function in silks. Curr Opinion Solid State Mater Sci 3(3):237–245CrossRefGoogle Scholar
  44. Jelinski LW, Blye A, Liivak O, Michal C, LaVerde G, Seidel A, Shah N, Yang Z (1999) Orientation, structure, wet-spinning, and molecular basis for supercontraction of spider dragline silk. Int J Biol Macromol 24(2):197–201CrossRefPubMedGoogle Scholar
  45. Jenkins JE, Creager MS, Butler EB, Lewis RV, Yarger JL, Holland GP (2010) Solid-state NMR evidence for elastin-like β-turn structure in spider dragline silk. Chem Commun 46(36):6714–6716CrossRefGoogle Scholar
  46. Joel AC, Kappel P, Adamova H, Baumgartner W, Scholz I (2015) Cribellate thread production in spiders: complex processing of nano-fibres into a functional capture thread. Arthropod Struct Dev 44(6):568–573CrossRefPubMedGoogle Scholar
  47. Köhler T, Vollrath F (1995) Thread biomechanics in the two orb-weaving spiders Araneus diadematus (Araneae, Araneidae) and Uloborus walckenaerius (Araneae, Uloboridae). J Exper Zool 271(1):1–7CrossRefGoogle Scholar
  48. Kullmann EJ (1972) The convergent development of orb-webs in cribellate and ecribellate spiders. Am Zool 12(3):395–405CrossRefGoogle Scholar
  49. Liao X, Yin G, Huang Z, Yao Y, Gu J, Han D (2011) Supercontraction on cribellate spider spiral silk with wet-rebuilt micro-structure. Mater Sci Eng C 31(2):128–133CrossRefGoogle Scholar
  50. Liu Y, Sponner A, Porter D, Vollrath F (2007) Proline and processing of spider silks. Biomacromolecules 9(1):116–121CrossRefPubMedGoogle Scholar
  51. Liu Y, Shao ZZ, Vollrath F (2008) Elasticity of spider silks. Biomacromolecules 9:1782–1786CrossRefPubMedGoogle Scholar
  52. Lombardi SJ, Kaplan DL (1990) The amino acid composition of major ampullate gland silk (dragline) of Nephila clavipes (Araneae, Tetragnathidae). J Arachnol 297–306Google Scholar
  53. Marhabaie M, Leeper TC, Blackledge TA (2014) Protein composition correlates with the mechanical properties of spider (Argiope trifasciata) dragline silk. Biomacromolecules 15:20–29CrossRefPubMedGoogle Scholar
  54. Opell BD (1994) Factors governing the stickiness of cribellar prey capture threads in the spider family Uloboridae. J Morph 221:111–119CrossRefGoogle Scholar
  55. Opell BD (1997) The material cost and stickiness of capture threads and the evolution of orb-weaving spiders. Biol J Linn Soc 62(3):443–458CrossRefGoogle Scholar
  56. Opell BD (1999) Redesigning spider webs: stickiness, capture area, and the evolution of modern orb-webs. Evolutionary Ecol Res 1:503–516Google Scholar
  57. Opell BD, Bond JE (2000) Capture thread extensibility of orb-weaving spiders: testing punctuated and associative explanations of character evolution. Biol J Linn Soc 70(1):107–120CrossRefGoogle Scholar
  58. Opell BD, Bond JE (2001) Changes in the mechanical properties of capture threads and the evolution of modern orb-weaving spiders. Evol Ecol Res 3(5):507–519Google Scholar
  59. Opell BD, Hendricks ML (2007) Adhesive recruitment by the viscous capture threads of araneoid orb-weaving spiders. J Exper Biol 210:553–560CrossRefGoogle Scholar
  60. Opell BD, Schwend HS (2009) Adhesive efficiency of spider prey capture threads. Zoology 112(1):16–26CrossRefPubMedGoogle Scholar
  61. Opell BD, Karinshak SE, Sigler MA (2011a) Humidity affects the extensibility of an orb-weaving spider's viscous thread droplets. J Exper Biol 214(17):2988–2993CrossRefGoogle Scholar
  62. Opell BD, Tran AM, Karinshak SE (2011b) Adhesive compatibility of cribellar and viscous prey capture threads and its implication for the evolution of orb-weaving spiders. J Exper Zool Part A: Ecol Genet Phys 315(6):376–384CrossRefGoogle Scholar
  63. Perea GB, Riekel C, Guinea GV, Madurga R, Daza R, Burghammer M, Hayashi C, Elices M, Plaza GR, Pérez-Rigueiro J. (2013) Identification and dynamics of polyglycine II nanocrystals in Argiope trifasciata flagelliform silk. Sci Rep 3. doi:  10.1038/srep03061
  64. Pérez-Rigueiro J, Elices M, Plaza G, Real JI, Guinea GV (2005) The effect of spinning forces on spider silk properties. J Exper Biol 208(14):2633–2639CrossRefGoogle Scholar
  65. Peters HM (1987) Fine structure and function of capture threads. In: Ecophysiology of spiders, 187–202. Springer Berlin HeidelbergGoogle Scholar
  66. Plaza GR, Guinea GV, Pérez-Rigueiro J, Elices M (2006) Thermo-hygro-mechanical behavior of spider dragline silk: glassy and rubbery states. J Polymer Sci B: Polymer Phys 44(6):994–999CrossRefGoogle Scholar
  67. Sahni, V, Blackledge TA, Dhinojwala A (2010) Viscoelastic solids explain spider web stickiness. Nat Commun 1. doi:  10.1038/ncomms1019
  68. Savage KN, Gosline JM (2008) The role of proline in the elastic mechanism of hydrated spider silks. J Exper Biol 211(12):1948–1957CrossRefGoogle Scholar
  69. Sensenig A, Agnarsson I, Blackledge TA (2010) Behavioural and biomaterial coevolution in spider orb webs. J Evol Biol 23(9):1839–1856CrossRefPubMedGoogle Scholar
  70. Shao Z, Young RJ, Vollrath F (1999) The effect of solvents on spider silk studied by mechanical testing and single-fibre Raman spectroscopy. Int J Biol Macromol 24(2):295–300CrossRefPubMedGoogle Scholar
  71. Swanson BO, Blackledge TA, Beltrán J, Hayashi CY (2006) Variation in the material properties of spider dragline silk across species. Appl Phys A 82(2):213–218CrossRefGoogle Scholar
  72. Swanson BO, Blackledge TA, Hayashi CY (2007) Spider capture silk: performance implications of variation in an exceptional biomaterial. J Exper Zool A Ecol Genet Physiol 307:654–666CrossRefGoogle Scholar
  73. Termonia Y (1994) Molecular modeling of spider silk elasticity. Macromolecules 27(25):7378–7381CrossRefGoogle Scholar
  74. Vollrath F, Edmonds D (1989) Modulation of the mechanical properties of spider silk by coating with water. Nature 340:305–307CrossRefGoogle Scholar
  75. Work RW (1976) The force-elongation behavior of web fibers and silks forcibly obtained from orb-web-spinning spiders. Text Res J 46(7):485–492CrossRefGoogle Scholar
  76. Work RW, Young CT (1987) The amino acid compositions of major and minor ampullate silks of certain orb-web-building spiders (Araneae, Araneidae). J Arachnol 65–80Google Scholar
  77. Yang Z, Liivak O, Seidel A, LaVerde G, Zax DB, Jelinski LW (2000) Supercontraction and backbone dynamics in spider silk: 13C and 2H NMR studies. J Amer Chem Soc 122(37):9019–9025CrossRefGoogle Scholar
  78. Zeileis A (2004) Econometric computing with HC and HAC covariance matrix estimators. J Stat Softw 11(10):1–17 URL: CrossRefGoogle Scholar
  79. Zschokke S, Vollrath F (1995) Unfreezing the behaviour of two orb spiders. Phys Behav 58(6):1167–1173CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of BiologyThe University of AkronAkronUSA
  2. 2.Department of Life ScienceTunghai UniversityTaichungTaiwan
  3. 3.Department of Biology, Integrated Bioscience ProgramThe University of AkronAkronUSA

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