Todd A. Blackledge

Reconstructing web evolution and spider diversification in the molecular era

The evolutionary diversification of spiders is attributed to spectacular innovations in silk. Spiders are unique in synthesizing many different kinds of silk, and using silk for a variety of ecological functions throughout their lives, particularly to make prey-catching webs. Here, we construct a broad higher-level phylogeny of spiders combining molecular data with traditional morphological and behavioral characters. We use this phylogeny to test the hypothesis that the spider orb web evolved only once. We then examine spider diversification in relation to different web architectures and silk use. We find strong support for a single origin of orb webs, implying a major shift in the spinning of capture silk and repeated loss or transformation of orb webs. We show that abandonment of costly cribellate capture silk correlates with the 2 major diversification events in spiders (1). Replacement of cribellate silk by aqueous silk glue may explain the greater diversity of modern orb-weaving spiders (Araneoidea) compared with cribellate orb-weaving spiders (Deinopoidea) (2). Within the “RTA clade,” which is the sister group to orb-weaving spiders and contains half of all spider diversity, >90% of species richness is associated with repeated loss of cribellate silk and abandonment of prey capture webs. Accompanying cribellum loss in both groups is a release from substrate-constrained webs, whether by aerially suspended webs, or by abandoning webs altogether. These behavioral shifts in silk and web production by spiders thus likely played a key role in the dramatic evolutionary success and ecological dominance of spiders as predators of insects.

Silken Toolkits: Biomechanics of Silk Fibers Spun by the Orb Web Spider Argiope Argentata (Fabricius 1775)

SUMMARY Orb-weaving spiders spin five fibrous silks from differentiated glands that contain unique sets of proteins. Despite diverse ecological functions, the mechanical properties of most of these silks are not well characterized. Here, we quantify the mechanical performance of this toolkit of silks for the silver garden spider Argiope argentata. Four silks exhibit viscoelastic behaviour typical of polymers, but differ statistically from each other by up to 250% in performance, giving each silk a distinctive suite of material properties. Major ampullate silk is 50% stronger than other fibers, but also less extensible. Aciniform silk is almost twice as tough as other silks because of high strength and extensibility. Capture spiral silk, coated with aqueous glue, is an order of magnitude stretchier than other silks. Dynamic mechanical properties are qualitatively similar, but quantitatively vary by up to 300% among silks. Storage moduli are initially nearly constant and increase after fiber yield, whereas loss tangents reach maxima of 0.1–0.2 at the yield. The remarkable mechanical diversity of Argiope argentata silks probably results in part from the different molecular structures of fibers and can be related to the specific ecological role of each silk. Our study indicates substantial potential to customize the mechanics of bioengineered silks.

Viscoelastic solids explain spider web stickiness

Modern orb-weaving spiders have evolved well-designed adhesives to capture preys. This adhesive is laid on a pair of axial silk fibres as micron-sized glue droplets that are composed of an aqueous coat of salts surrounding nodules made of glycoproteins. In this study, we measure the adhesive forces required to separate a small microscopic probe after bringing it in contact with a single glue droplet. These forces are highly rate-dependent and are two orders of magnitude higher than the capillary forces. The glycoproteins in the glue droplets behave as a viscoelastic solid and the elasticity is critical in enhancing adhesion caused by specific adhesive ligands. These results have important implications in mimicking bioadhesives.

The Form and Function of Spider Orb Webs: Evolution from Silk to Ecosystems

Spiders are the preeminent silk craftsmen among arthropods and are best known for producing aerial orb webs that snare flying insects. Orb web spiders are ubiquitous predators in terrestrial ecosystems and are popular models for behavioural and ecological research, in part due to the ease of characterizing the shapes of orb webs. Orb webs are composite structures built from multiple types of silks, each with its own unique molecular structure and mechanical function, such that orb webs also link together evolutionary research from the genes coding for silk proteins to whole web function in the environment. Yet, orb webs are only intermediate structures in the evolutionary diversification of silk use among spiders, acting as stepping stones facilitating the origin of new web types and increased spider diversification. Here, we review the current research on the form and function of spider orb webs. We provide a comprehensive introduction to all aspects of orb web biology, suitable for any new investigation into orb web biology. While other reviews exist individually for webs, silk, and spider evolution, we hope that the synthetic nature of this review will facilitate a more integrated approach by future investigators. Finally, we explore in more detail some of the most dynamic areas of orb web biology to suggest promising venues for the next decade of research on these fascinating creatures and their silken snares. In particular, we discuss how spider webs might drive speciation, the dramatic growth in our understanding of the molecular ecology of spider silk, and the importance of a greater role for spider biology per se in silk biomimicry.

Behavioural and biomaterial coevolution in spider orb webs

Mechanical performance of biological structures, such as tendons, byssal threads, muscles, and spider webs, is determined by a complex interplay between material quality (intrinsic material properties, larger scale morphology) and proximate behaviour. Spider orb webs are a system in which fibrous biomaterials—silks—are arranged in a complex design resulting from stereotypical behavioural patterns, to produce effective energy absorbing traps for flying prey. Orb webs show an impressive range of designs, some effective at capturing tiny insects such as midges, others that can occasionally stop even small birds. Here, we test whether material quality and behaviour (web design) co‐evolve to fine‐tune web function. We quantify the intrinsic material properties of the sticky capture silk and radial support threads, as well as their architectural arrangement in webs, across diverse species of orb‐weaving spiders to estimate the maximum potential performance of orb webs as energy absorbing traps. We find a dominant pattern of material and behavioural coevolution where evolutionary shifts to larger body sizes, a common result of fecundity selection in spiders, is repeatedly accompanied by improved web performance because of changes in both silk material and web spinning behaviours. Large spiders produce silk with improved material properties, and also use more silk, to make webs with superior stopping potential. After controlling for spider size, spiders spinning higher quality silk used it more sparsely in webs. This implies that improvements in silk quality enable ‘sparser’ architectural designs, or alternatively that spiders spinning lower quality silk compensate architecturally for the inferior material quality of their silk. In summary, spider silk material properties are fine‐tuned to the architectures of webs across millions of years of diversification, a coevolutionary pattern not yet clearly demonstrated for other important biomaterials such as tendon, mollusc byssal threads, and keratin.

SILK MEDIATED DEFENSE BY AN ORB WEB SPIDER AGAINST PREDATORY MUD-DAUBER WASPS

Stabilimenta are zigzag and spiral designs of seemingly conspicuous silk included at the centers of many spider webs. We examined the association of stabilimenta with the ability of spiders to defend themselves against predatory mud-dauber wasps. We found that Argiope trifasciata (Araneae, Araneidae) were significantly more likely to survive attacks by Chalybion caeruleum and Sceliphron caementarium (Hymenoptera, Sphecidae) when spiders included stabilimenta in webs. This association could not be explained by factors such as differences in sizes or conditions of spiders nor locations of webs. We suggest that stabilimenta may function to delay pursuit of spiders as they drop from webs by physically blocking wasps, camouflaging spiders or distracting attacking wasps. Stabilimenta may function in a role very similar to the retreats built by many other genera of spiders and appear to be an adaptation to reduce the predation pressure faced by spiders that have evolved foraging habits at highly exposed diurnal web sites.

Spider silk as a novel high performance biomimetic muscle driven by humidity

SUMMARY The abrupt halt of a bumble bees flight when it impacts the almost invisible threads of an orb web provides an elegant example of the amazing strength and toughness of spider silk. Spiders depend upon these properties for survival, yet the impressive performance of silk is not limited solely to tensile mechanics. Here, we show that silk also exhibits powerful cyclic contractions, allowing it to act as a high performance mimic of biological muscles. These contractions are actuated by changes in humidity alone and repeatedly generate work 50 times greater than the equivalent mass of human muscle. Although we demonstrate that this response is general and occurs weakly in diverse hydrophilic materials, the high modulus of spider silk is such that it generates exceptional force. Furthermore, because this effect already operates at the level of single silk fibers, only 5 μm in diameter, it can easily be scaled across the entire size range at which biological muscles operate. By contrast, the most successful synthetic muscles developed so far are driven by electric voltage, such that they cannot scale easily across large ranges in cross-sectional areas. The potential applicability of silk muscles is further enhanced by our finding that silkworm fibers also exhibit cyclic contraction because they are already available in commercial quantities. The simplicity of using wet or dry air to drive the biomimetic silk muscle fibers and the incredible power generated by silk offer unique possibilities in designing lightweight and compact actuators for robots and micro-machines, new sensors, and green energy production.

Unraveling the Mechanical Properties of Composite Silk Threads Spun by Cribellate Orb-Weaving Spiders

SUMMARY Orb-web weaving spiders depend upon the mechanical performance of capture threads to absorb the energy of flying prey. Most orb-weavers spin wet capture threads with core fibers of flagelliform silk. These threads are extremely compliant and extensible due to the folding of their constituent proteins into molecular nanosprings and hydration by a surrounding coating of aqueous glue. In contrast, other orb-weavers use cribellate capture threads, which are composite structures consisting of core fibers of pseudoflagelliform silk surrounded by a matrix of fine dry cribellar fibrils. Based on phylogenetic evidence, cribellate capture threads predate the use of viscid capture threads. To better characterize how pseudoflagelliform and cribellar fibrils function, we investigated the mechanical performance of cribellate capture threads for three genera of spiders (Deinopis, Hyptiotes and Uloborus). These taxa spin very diverse web architectures, ranging from complete orbs to evolutionarily reduced triangle webs and cast nets. We found that the pseudoflagelliform core fibers of these webs were stiffer and stronger, but also less extensible, than flagelliform silk. However, cribellate capture threads achieved overall high extensibilities because the surrounding cribellar fibrils contributed substantially to the tensile performance of threads long after the core pseudoflagelliform fibers ruptured. In the case of Deinopis capture threads, up to 90% of the total work performed could be attributed to these fibrils. These findings yield insight into the evolutionary transition from cribellate to viscid capture threads.

SPIDER DRAGLINE SILK: CORRELATED AND MOSAIC EVOLUTION IN HIGH-PERFORMANCE BIOLOGICAL MATERIALS

Abstract The evolution of biological materials is a critical, yet poorly understood, component in the generation of biodiversity. For example, the diversification of spiders is correlated with evolutionary changes in the way they use silk, and the material properties of these fibers, such as strength, toughness, extensibility, and stiffness, have profound effects on ecological function. Here, we examine the evolution of the material properties of dragline silk across a phylogenetically diverse sample of species in the Araneomorphae (true spiders). The silks we studied are generally stronger than other biological materials and tougher than most biological or man-made fibers, but their material properties are highly variable; for example, strength and toughness vary more than fourfold among the 21 species we investigated. Furthermore, associations between different properties are complex. Some traits, such as strength and extensibility, seem to evolve independently and show no evidence of correlation or trade-off across species, even though trade-offs between these properties are observed within species. Material properties retain different levels of phylogenetic signal, suggesting that traits such as extensibility and toughness may be subject to different types or intensities of selection in several spider lineages. The picture that emerges is complex, with a mosaic pattern of trait evolution producing a diverse set of materials across spider species. These results show that the properties of biological materials are the target of selection, and that these changes can produce evolutionarily and ecologically important diversity.

Quasistatic and Continuous Dynamic Characterization of the Mechanical Properties of Silk from the Cobweb of the Black Widow Spider Latrodectus Hesperus

SUMMARY Spider silks are among the strongest and toughest known materials, but investigation of these remarkable properties has been confined largely to orb-weaving spiders. We investigated the mechanical performance of silk from the cobweb-weaving spider Latrodectus hesperus. Both silk from the scaffolding region of the web and sticky gumfooted capture lines had material properties similar to the major ampullate silk that orb weavers use as the framework for their orb webs. Major ampullate fibers obtained from anaesthetized Latrodectus spiders were similar, but exhibited increased stiffness and reduced extensibility. Novel continuous dynamic analysis of the silks revealed that the loss tangent (tanδ) increased rapidly during the first 2-3% of extension and reached a maximum near the yield point of fibers. The loss tangent then rapidly declined at an ever-decreasing rate until failure. We suggest that these data support molecular models for the mechanics of spider silk. We also demonstrate that the addition of sticky aggregate glue to the ends of the gumfooted lines modulates their mechanical performance - reducing stiffness and increasing extensibility. The storage modulus of viscid regions of the gumfooted lines was much lower than dry regions. This may be explained by disruption of hydrogen bonding within the amorphous regions of the fibers due to hydration from the glue.