Connecting materials, performance and evolution: a case study of the glue of moth-catching spiders (Cyrtarachninae)

Abstract

Morphological structures and extended phenotypes are made possible by materials that are encoded by the genome. Nearly all biomaterials are viscoelastic, which means that to understand performance, one must understand the strain rate-dependent properties of these materials in relevant ecological interactions, as the behavior of a material can vary dramatically and rapidly. Spider silks are an example of materials whose properties vary substantially intra- and inter-specifically. Here, we focus on aggregate silk, which functions as a biological adhesive. As a case study to understand how a material manifests from genome through organism to ecology, we highlight moth-specialist spiders, the Cyrtarachninae, and their glues as an ideal experimental system to investigate the relationship between genomics and ecologically variable performance of a biological material. There is a clear eco-evolutionary innovation that Cyrtarachne akirai and related species have evolved, a unique trait not found in other spiders, a glue which overcomes the scales of moths. By examining traditional orb-weavers, C. akirai and other subfamily members using biomechanical testing and genomic analysis, we argue that we can track the evolution of this novel bioadhesive and comment on the selection pressures influencing prey specialization. The importance of the ecological context of materials testing is exemplified by the poor performance of C. akirai glue on glass and the exceptional spreading ability and adhesive strength on moths. The genetic basis for these performance properties is experimentally tractable because spider silk genes are minimally pleiotropic and advances in genomic technologies now make possible the discovery of complete silk gene sequences.

The evolutionary history of cribellate orb-weaver capture thread spidroins

“…Both genes are comprised of distinct repeats arranged in a stereotypical pattern. The occurrence of hierarchically organized repetitive units (i.e., ensemble repeats) has been found in other spidroins such as MaSp1 [ 75 ] and AgSp [ 99 , 100 ] suggesting they may be critical to the mechanical performance of these proteins. Similarly, comparison of the U. diversus sequences with Octonoba reveals shared repetitive features that may have functional significance.…”

Rapid molecular diversification and homogenization of clustered major ampullate silk genes in Argiope garden spiders

“…Even for highly repetitive proteins, it is rare for the repeat region to comprise nearly all of the amino acid sequence [100], as is the case for spidroins. Similar to some other repetitive proteins [105][106][107][108][109], spidroin repetitive sequence is often organized in a hierarchical fashion with smaller repeats nested within a larger repeat unit [47,48,53,110]. In addition, spidroins generally exhibit extreme homogenization across repeat units [15,46,47,[111][112][113].…”

Behavior and Bioadhesives: How Bolas Spiders, Mastophora hutchinsoni, Catch Moths

“…In whichever form this prediction is stated, it represents the physical requirements for the behavior. Moreover, the first form of the prediction places these physical requirements into the phylogenetic context of the moth-catching specialists in the Cyrtarachninae, a taxon that has evolved a diversity of ways to catch moths, all of which involve correlated changes in web architecture, silk material properties, and behavior [12].…”

“…This glue penetrates not only the top layer of scales but also glues them to the cuticle below [4]. As it spreads, this glue hardens and dries, a behavior not seen in the glues of traditional orb-weaving species [4,8,9,11,12]. For this genus and a few others, the ability to catch moths comes with a trade-off in that web spinning is limited to environmental conditions with relative humidity (RH) at or above 80% [8,9,13].…”