Evolution of Silk Anchor Structure as the Joint Effect of Spinning Behavior and Spinneret Morphology

Abstract

Synopsis Spider web anchors are attachment structures composed of the bi-phasic glue-fiber secretion from the piriform silk glands. The mechanical performance of the anchors strongly correlates with the structural assembly of the silk lines, which makes spider silk anchors an ideal system to study the biomechanical function of extended phenotypes and its evolution. It was proposed that silk anchor function guided the evolution of spider web architectures, but its fine-structural variation and whether its evolution was rather determined by changes of the shape of the spinneret tip or in the innate spinning choreography remained unresolved. Here, we comparatively studied the micro-structure of silk anchors across the spider tree of life, and set it in relation to spinneret morphology, spinning behavior and the ecology of the spider. We identified a number of apomorphies in the structure of silk anchors that may positively affect anchor function: (1) bundled dragline, (2) dragline envelope, and (3) dragline suspension (“bridge”). All these characters were apomorphic and evolved repeatedly in multiple lineages, supporting the notion that they are adaptive. The occurrence of these structural features can be explained with changes in the shape and mobility of the spinneret tip, the spinning behavior, or both. Spinneret shapes generally varied less than their fine-tuned movements, indicating that changes in construction behavior play a more important role in the evolution of silk anchor assembly. However, the morphology of the spinning apparatus is also a major constraint to the evolution of the spinning choreography. These results highlight the changes in behavior as the proximate and in morphology as the ultimate causes of extended phenotype evolution. Further, this research provides a roadmap for future bioprospecting research to design high-performance instant line anchors.