Material properties of evolutionary diverse spider silks described by variation in a single structural parameter

Abstract

Spider major ampullate gland silks (MAS) vary greatly in material properties among species but, this variation is shown here to be confined to evolutionary shifts along a single universal performance trajectory. This reveals an underlying design principle that is maintained across large changes in both spider ecology and silk chemistry. Persistence of this design principle becomes apparent after the material properties are defined relative to the true alignment parameter, which describes the orientation and stretching of the protein chains in the silk fiber. Our results show that the mechanical behavior of all Entelegynae major ampullate silk fibers, under any conditions, are described by this single parameter that connects the sequential action of three deformation micromechanisms during stretching: stressing of protein-protein hydrogen bonds, rotation of the β-nanocrystals and growth of the ordered fraction. Conservation of these traits for over 230 million years is an indication of the optimal design of the material and gives valuable clues for the production of biomimetic counterparts based on major ampullate spider silk.

Figure 1. Tensile properties of Nephila inaurata MAS.

(A) Range of tensile properties of N. inaurata MAS expressed as true stress-true strain curves. (B) The use of the alignment parameter, α, allows classifying the full range of true stress-true strain curves measured from N. inaurata MAS. (C) The use of the true alignment parameter, α_T, allows defining the overall tensile behavior of N. inaurata MAS in terms of true stress-true strain curves. Each curve is displaced along the true strain axis (X axis) by α_T taken the MS curve (α_T = 0) as reference. (D) Same as in (C) but including the true stress-true strain curve of N. inaurata MAS tested in water (discontinuous line) and displaced along the true stress axis (Y axis). The value of the displacement is such that the true stress of the displaced curve at the origin (ε = 0) concurs with the yield stress of the MS fiber tested in air.

Figure 2. Tensile properties of MAS spun by representatives of the Entelegynae group.

(A) Concurring tensile behavior of MAS spun by Entelegynae spiders after maximum supercontraction. Argiope aurantia maximum supercontracted MAS is used as reference. The interspecific true alignment parameter, α_Τ0, is defined as the true strain at zero true stress of the curves of any species. A.a.: Argiope aurantia, D.s.: Deinopis spinosa, C.d: Caerostris darwini, A.l.: Argiope lobata, L.h.: Latrodectus hesperus, D.t.: Dolomedes tenebrosus, T.r.: Tengella radiata, P.r.: Phidippus regius. (B) Definition of α^*_T in terms of α_T0 and α_T. α_Τ0(N.i.) labels the interspecific alignment parameter of the MS state of N. inaurata. Also represented is the value of α^*_T for N. inaurata fibers with a value of the true alignment parameter of α_T = 0.4 (Fig. 1C). The value of the interspecific alignment parameter is calculated as α^*_T = α_Τ0(N.i.) + α_T. (C) Concurring tensile behavior of stretched MAS. The general interspecific alignment parameter, α^*_T, is provided below the species identification defined as α^*_T = α_Τ0(MS) + α_T. N.i.: Nephila inaurata, A.t.: Argiope trifasciata, A.l.: Argiope lobata, A.b.: Argiope bruennichi.

Figure 3. Correlation between elastic modulus (A) and yield stress (B) with the values of the interspecific alignment parameter, α_T0.

Figure 4. Summary of the microdeformation mechanisms and motifs of sequence of MAS and their relationship with the true alignment parameter, α^*_T.