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

Abstract

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.

Tuning orb spider glycoprotein glue performance to habitat humidity

“…Finally, did the hygroscopicity system arise to help spiders conserve water resources after viscid glue was already being produced (e.g. the ancestral condition was for orb spiders to exude wet sticky secretions from their aggregate glands) or as a mechanism to improve adhesion (Opell et al, 2011b;Piorkowski and Blackledge, 2017) with spiders adding LMMCs to dry adhesive secretions for some other functional benefit?…”

“…7). Moreover, as force is applied to a thread, the extension of its droplets and flagelliform lines combines to dissipate the energy of a struggling prey (Piorkowski and Blackledge, 2017;Sahni et al, 2011). Thus, there are two ways to characterize viscous thread adhesion: the force required to pull a thread from a surface (e.g.…”

“…When threads were stretched experimentally to reduce axial fiber extensibility, but the number of contributing droplets was maintained by contacting longer thread lengths, the force required to pull a thread from a surface decreased . Flagelliform fiber extension is also crucial for a thread's ability to dissipate the energy of a struggling insect (Sahni et al, 2011), contributing more than twice the work of adhesion as combined droplet extensions (Piorkowski and Blackledge, 2017).…”

Linking properties of an orb‐weaving spider's capture thread glycoprotein adhesive and flagelliform fiber components to prey retention time

“…Capture thread adhesion has been characterized in two ways: (a) the force required to pull a thread or one of its glue droplets from a surface (Opell & Hendricks, ; Opell, Karinshak, & Sigler, ) and (b) the work done in pulling a thread or glue droplet from a surface (Opell, Clouse, & Andrews, ; Piorkowski & Blackledge, ; Sahni, Blackledge, & Dhinojwala, ). The latter approach probably best characterizes a thread's ability to overcome the work of an ensnared insect as it struggles to escape from a web.…”

Elastic modulus and toughness of orb spider glycoprotein glue

“…These curves also permitted us to determine the glycoprotein core’s toughness, the work required to extend the material to rupture, or, in the case of viscous threads droplets, pull-off from a contacted surface. This is an important index because droplet and axial line extension dissipate the energy of an insect’s struggles to escape from a web [ 43 ].…”