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 preycatching 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.Araneidae ͉ behavioral evolution ͉ cribellate silk ͉ orb web ͉ speciation S piders are exceptionally diverse and abundant in terrestrial ecosystems. In contrast to megadiverse orders of insects, evolutionary diversification of spiders is not coupled with major trophic shifts. All spiders are predators of arthropods, and spiders are dominant consumers at intermediate trophic levels (1, 2). Spider diversification is instead linked to key innovations in silk use (3-7). For instance, the araneoid orb web (Fig. 1) with stretchy capture spirals, coated by adhesive viscid silk secretions, provides access to abundant flying insects (3,8). However, many spiders produce cribellate silk, a radically different dry adhesive that adheres to prey, using van der Waals interactions and hygroscopic forces (9). Some cribellate spiders also construct aerial orb webs, whereas most spin sheet-like webs on the substrate (Fig. S1) or have abandoned capture webs altogether. Furthermore, the most diverse families within ''orb-weavers'' (Orbiculariae) no longer build orb webs, but instead spin aerial sheet webs (Linyphiidae) or cobwebs (Theridiidae) (Fig. S2). Thus, discovering the pattern of evolution of web spinning behaviors is essential for understanding spider diversification.Orb webs possessing dry cribellate capture spirals are architecturally similar to those spun from aqueous viscid silk ( Fig. 1 ...

BackgroundCombining high strength and elasticity, spider silks are exceptionally tough, i.e., able to absorb massive kinetic energy before breaking. Spider silk is therefore a model polymer for development of high performance biomimetic fibers. There are over 41.000 described species of spiders, most spinning multiple types of silk. Thus we have available some 200.000+ unique silks that may cover an amazing breadth of material properties. To date, however, silks from only a few tens of species have been characterized, most chosen haphazardly as model organisms (Nephila) or simply from researchers' backyards. Are we limited to ‘blindly fishing’ in efforts to discover extraordinary silks? Or, could scientists use ecology to predict which species are likely to spin silks exhibiting exceptional performance properties?MethodologyWe examined the biomechanical properties of silk produced by the remarkable Malagasy ‘Darwin's bark spider’ (Caerostris darwini), which we predicted would produce exceptional silk based upon its amazing web. The spider constructs its giant orb web (up to 2.8 m2) suspended above streams, rivers, and lakes. It attaches the web to substrates on each riverbank by anchor threads as long as 25 meters. Dragline silk from both Caerostris webs and forcibly pulled silk, exhibits an extraordinary combination of high tensile strength and elasticity previously unknown for spider silk. The toughness of forcibly silked fibers averages 350 MJ/m3, with some samples reaching 520 MJ/m3. Thus, C. darwini silk is more than twice tougher than any previously described silk, and over 10 times better than Kevlar®. Caerostris capture spiral silk is similarly exceptionally tough.Conclusions Caerostris darwini produces the toughest known biomaterial. We hypothesize that this extraordinary toughness coevolved with the unusual ecology and web architecture of these spiders, decreasing the likelihood of bridgelines breaking and collapsing the web into the river. This hypothesis predicts that rapid change in material properties of silk co-occurred with ecological shifts within the genus, and can thus be tested by combining material science, behavioral observations, and phylogenetics. Our findings highlight the potential benefits of natural history–informed bioprospecting to discover silks, as well as other materials, with novel and exceptional properties to serve as models in biomimicry.

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.

Araneoid spiders use specialized abdominal glands to produce up to seven different protein-based silks/glues that have diverse physical properties. The fibroin sequences that encode aciniform fibers (wrapping silk) and the mechanical properties of these fibers have not been characterized previously. To gain a better understanding of the molecular radiation of spider silk fibroin genes, cDNA libraries derived from aciniform glands of the banded garden spider, Argiope trifasciata, were constructed, and unique silk transcripts were sequenced. There was evidence for a single silk fibroin gene that was expressed in the aciniform glands, and the inferred amino acid composition of the novel fibroin closely matched the amino acid contents of these glands. The inferred protein, aciniform spidroin 1 (AcSp1), is composed of highly homogenized repeats that are 200 amino acids in length. The long stretches of poly-alanine and glycine-alanine subrepeats, which are thought to account for the crystalline regions of minor ampullate and major ampullate fibers, are very poorly represented in AcSp1. The AcSp1 repeat unit is iterated minimally 14 times and does not display substantial sequence similarity to any previously described genes or proteins. Database searches, however, showed that the nonrepetitive carboxy-terminus contains stretches of matches to known spider fibroin sequences, suggesting that the AcSp1 gene is a highly divergent member of the spider silk gene family. In phylogenetic analyses of carboxy-terminal sequences from araneid spiders, the aciniform sequence did not group strongly with clusters of fibroins from the flagelliform, minor ampullate, or major ampullate silk glands. Comparisons of stress/strain curves for major ampullate, minor ampullate, and aciniform silks from Argiope trifasciata showed significant differences in ultimate strength, extensibility, and toughness. Remarkably, the toughness of aciniform silk was 50% greater than the highest values typically recorded for major ampullate silk. These differences in performance, in combination with the radical divergence at the sequence level among fibroin paralogs, suggest a possible linkage between silk fibroin sequences and performance that should be explored in future structural/functional studies of aciniform silk.

Modern orb-weaving spiders have evolved well-designed adhesives to capture preys. This adhesive is laid on a pair of axial silk fi bres 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 specifi c adhesive ligands. These results have important implications in mimicking bioadhesives.

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.

Adhesion in humid conditions is a fundamental challenge to both natural and synthetic adhesives. Yet, glue from most spider species becomes stickier as humidity increases. We find the adhesion of spider glue, from five diverse spider species, maximizes at very different humidities that matches their foraging habitats. By using high-speed imaging and spreading power law, we find that the glue viscosity varies over 5 orders of magnitude with humidity for each species, yet the viscosity at maximal adhesion for each species is nearly identical, 10(5)-10(6) cP. Many natural systems take advantage of viscosity to improve functional response, but spider glue's humidity responsiveness is a novel adaptation that makes the glue stickiest in each species' preferred habitat. This tuning is achieved by a combination of proteins and hygroscopic organic salts that determines water uptake in the glue. We therefore anticipate that manipulation of polymer-salts interaction to control viscosity can provide a simple mechanism to design humidity responsive smart adhesives.

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