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.
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Connecting materials, performance and evolution: a case study of the glue of moth-catching spiders (Cyrtarachninae)
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.
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- Award ID(s):
- 2031962
- NSF-PAR ID:
- 10356474
- Date Published:
- Journal Name:
- Journal of experimental biology
- Volume:
- 225
- Issue:
- suppl_1
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Spiders use various combinations of silks, adhesives, and behaviors to ensnare and trap prey. A common but difficult to catch prey in most spider habitats are moths. They easily escape typical orb-webs because their bodies are covered in sacrificial scales that flake off when in contact with the web’s adhesives. This defense is defeated by spiders of the sub-family of Cyrtarachninae, moth-catching specialists who combine changes in orb-web structure, predatory behavior, and chemistry of the aggregate glue placed in those webs. The most extreme changes in web structure are shown by bolas spiders, who create a solitary capture strand containing only one or two glue droplets at the end of a single thread. They prey on male moths by releasing pheromones to draw them within range of their bolas, which they flick to ensnare the moth. We used a high-speed video camera to capture the behavior of the bolas spider Mastophora hutchinsoni. We calculated the kinematics of spiders and moths in the wild to model the physical and mechanical properties of the bolas during prey capture, the behavior of the moth, and how these factors lead to successful prey capture. We created a numerical model to explain the mechanical behavior of the bolas silk during prey capture. Our kinematic analysis shows that the material properties of the aggregate glue bolas of M. hutchinsoni are distinct from that of the other previously analyzed moth-specialist, Cyrtarachne akirai. The spring-like behavior of the M. hutchinsoni bolas suggests it spins a thicker liquid.
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null (Ed.)Abstract The origin of aggregate silk glands and their production of wet adhesive silks is considered a key innovation of the Araneoidea, a superfamily of spiders that build orb-webs and cobwebs. Orb-web weavers place aggregate glue on an extensible capture spiral, whereas cobweb weavers add it to the ends of strong, stiff fibers, called gumfoot lines. Here we describe the material behavior and quantitative proteomics of the aggregate glues of two cobweb weaving species, the Western black widow, Latrodectus hesperus, and the common house spider, Parasteatoda tepidariorum. For each species respectively, we identified 48 and 33 proteins that were significantly more abundant in the portion of the gumfoot line with glue than in its fibers. These proteins were more highly glycosylated and phosphorylated than proteins found in silk fibers without glue, which likely explains aggregate glue stickiness. Most glue-enriched proteins were of anterior aggregate gland origin, supporting the hypothesis that cobweb weavers’ posterior aggregate glue is specialized for another function. We found that cobweb weaver glue droplets are stiffer and tougher than the adhesive of most orb-web weaving species. Attributes of gumfoot glue protein composition that likely contribute to this stiffness include the presence of multiple protein families with conserved cysteine residues, a bimodal distribution of isoelectric points, and families with conserved functions in protein aggregation, all of which should contribute to cohesive protein-protein interactions. House spider aggregate droplets were more responsive to humidity changes than black widow droplets, which could be mediated by differences in protein sequence, post-translational modifications, the non-protein components of the glue droplets, and/or the larger amount of aqueous material that surrounds the adhesive cores of their glue droplets.more » « less
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Abstract Spider viscid silk adheres to insects in orb webs and is a “smart-adhesive” that quickly changes droplet size, viscosity, and adhesiveness in response to atmospheric humidity. Different species of spiders “tune” water uptake to match the humidity of their foraging environments, achieving a similar “universal” viscosity that optimizes tradeoffs in spreading versus cohesive bulk energy needed to enhance adhesion. Too much water lowers viscosity so that the glue spreads well, but cohesive failure occurs easily, generating poor adhesion. However, the optimal viscosity model of adhesion is based on experiments using smooth glass. Here we test the hypothesis that a less viscous, “over-lubricated” glue, which shows poor adhesion on smooth glass, will be stickier on hairy insects because of its greater ability to spread across three-dimensional rough surfaces. We ran adhesion tests of the furrow spider (Larinioides cornutus [Clerck 1757]) viscid silk on honey bee (Apis mellifera) thorax, with and without hairs, in either high or medium humidity. Our results show that “over-lubricated” glue increases adhesion on hairy surfaces, performing equally as well as an optimally viscous glue.more » « less
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Introduction Orb web and cobweb weaving spiders in the superfamily Araneoidea are distinguished by their ability to make a chemically sticky aqueous glue in specialized aggregate silk glands. Aggregate glue is an environmentally responsive material that has evolved to perform optimally around the humidity at which a spider forages. Protein components and their post-translational modifications confer stickiness to the glue, but the identities of these proteins have not been described for orb web weavers. Methods Using biomechanics, gene expression data, and proteomics, we characterized the glue’s physical properties and molecular components in two congeners that live in different environments, Argiope argentata (dry southwest US) and Argiope trifasciata (humid southeast US). Results The droplets of A. argentata are less hygroscopic than those of A. trifasciata and have proportionately smaller viscoelastic protein cores, which incorporate a smaller percentage of absorbed water as humidity increases. Argiope argentata protein cores were many times stiffer and tougher than A. trifasciata protein cores. Each species’ glue included ~30 aggregate-expressed proteins, most of which were homologous between the two species, with high sequence identity. However, the relative contribution and number of gene family members of each homologous group differed. For instance, the aggregate spidroins (AgSp1 and AgSp2) accounted for nearly half of the detected glue composition in A. argentata , but only 38% in A. trifasciata . Additionally, AgSp1, which has highly negatively charged regions, was ~2X as abundant as the positively charged AgSp2 in A. argentata , but ~3X as abundant in A. trifasciata . As another example, A. argentata glue included 11 members of a newly discovered cysteine-rich gene family, versus 7 members in A. trifasciata . Discussion Cysteines form disulfide bonds that, combined with the higher potential for electrostatic interactions between AgSp1 and AgSp2, could contribute to the greater stiffness of A. argentata glue. The ability to selectively express different glue protein genes and/or to extrude their products at different rates provides a faster mechanism to evolve material properties than sequence evolution alone.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/doi.org/10.1242/jeb.243271
