Changes in the material properties of spider glue droplet proteins accompanied shifts in prey capture biomechanics as cobweb spiders diverged from their orb weaving ancestors.

ABSTRACT

Although descended from orb weavers, spiders in the family Theridiidae spin cobwebs whose sticky prey capture gumfoot lines extend from a silk tangle to a surface below. When a crawling insect contacts glue droplets at the bottom of a gumfoot line, the line's weak pyriform anchor releases, causing the taut line to contract, pulling the insect from the surface and making its struggles to escape ineffective. To determine if this change in prey capture biomechanics was accompanied by a change in the material properties of theridiid glue, we characterized the elastic modulus and toughness of the glue droplet proteins of four theridiid species at 20-90 % relative humidity and compared their properties with those of 13 orb weaving species in the families Tetragnathidae and Araneidae. Compared to orb weavers, theridiid glue proteins had low extensions per protein volume and low elastic modulus and toughness values. These differences are likely explained by the loss of tension on a gumfoot line when its anchor fails, which may prioritize glue droplet adhesion rather than extension. Similarities in theridiid glue droplet properties did not reflect these species' evolutionary relationships. Instead, they appear associated with differences in web architecture. Two species that had stiffer gumfoot support lines and longer and more closely spaced gumfoot lines also had stiffer glue proteins. These lines may store more energy, and, when their anchors release, require stiffer glue to resist the more forceful upward thrust of a prey. STATEMENT OF SIGNIFICANCE: When a crawling insect contacts glue droplets on a theridiid cobweb's gumfoot line, this taut line's anchor fails and the insect is hoisted upward, rendering its struggles to escape ineffective. This strategy contrasts with that of orb weaving ancestors, which rely on more closely spaced prey capture threads to intercept and retain flying insects. A comparison of the elastic modulus and toughness of gumfoot and orb web glue proteins shows that this change in prey capture biomechanics is associated with reductions in the stiffness and toughness of cobweb glue. Unlike orb web capture threads, whose droplets extend in a coordinated fashion to sum adhesive forces, gumfoot lines become untethered, which prioritizes glue droplet adhesive contact over glue droplet extension.