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Tuning Orb Spider Glycoprotein Glue Performance to Habitat Humidity Brent D

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Tuning Orb Spider Glycoprotein Glue Performance to Habitat Humidity Brent D © 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb161539. doi:10.1242/jeb.161539 REVIEW Tuning orb spider glycoprotein glue performance to habitat humidity Brent D. Opell1,*, Dharamdeep Jain2, Ali Dhinojwala2 and Todd A. Blackledge3 ABSTRACT abdomen’s ventral surface; and Opisthothelae, which have Orb-weaving spiders use adhesive threads to delay the escape of unsegmented abdomens and posterior spinnerets (Platnick and insects from their webs until the spiders can locate and subdue the Gertsch, 1976). Opisthothelae contains two infraorders: insects. These viscous threads are spun as paired flagelliform axial Mygalomorphae, which includes tarantula and trapdoor spiders ’ fibers coated by a cylinder of solution derived from the aggregate whose cheliceral fangs move parallel to the body s sagittal plane; and glands. As low molecular mass compounds (LMMCs) in the aggregate Araneomorphae, which contains over 95% of all living spider solution attract atmospheric moisture, the enlarging cylinder becomes species whose fangs move more perpendicularly to the sagittal plane. unstable and divides into droplets. Within each droplet an adhesive Araneomorphae origin coincided with the appearance of a cribellum, glycoprotein core condenses. The plasticity and axial line extensibility a spinning plate formed of thousands of spigots that produces the of the glycoproteins are maintained by hygroscopic LMMCs. These nanofibers of a dry, fuzzy capture thread termed cribellate thread (see compounds cause droplet volume to track changes in humidity and Glossary). Although some araneomorphs continue to spin cribellate glycoprotein viscosity to vary approximately 1000-fold over the course threads (Opell, 2013), most no longer do so, constructing webs that of a day. Natural selection has tuned the performance of glycoprotein are not sticky or, like jumping spiders and wolf spiders, abandoning cores to the humidity of a species’ foraging environment by altering the web use in favor of other hunting tactics. The first orb webs contained composition of its LMMCs. Thus, species from low-humidity habits cribellate threads but 110 million years ago members of the have more hygroscopic threads than those from humid forests. superfamily Araneoidea replaced these with moist viscous capture However, at their respective foraging humidities, these species’ threads (see Glossary) (Peñalver et al., 2006). These viscous threads glycoproteins have remarkably similar viscosities, ensuring optimal are considered a key innovation (Bond and Opell, 1998), droplet adhesion by balancing glycoprotein adhesion and cohesion. contributing to the diversity of this clade, which contains 26% of Optimal viscosity is also essential for integrating the adhesion force of all spider species and comprises 17 families of orb-weaving spiders multiple droplets. As force is transferred to a thread’s support line, and their descendants that spin webs with divergent architectures extending droplets draw it into a parabolic configuration, implementing (Blackledge et al., 2009a,b; Dimitrov et al., 2016; Hormiga and a suspension bridge mechanism that sums the adhesive force Griswold, 2014). generated over the thread span. Thus, viscous capture threads Organisms employ adhesive secretions for a variety of other extend an orb spider’s phenotype as a highly integrated complex of functions. For example, Polychaeta annelids construct protective ̌ large proteins and small molecules that function as a self-assembling, tubes from cemented sand particles (Pavlovic et al., 2014), barnacles highly tuned, environmentally responsive, adhesive biomaterial. cement their cases to rocks and mussels attach themselves by byssal Understanding the synergistic role of chemistry and design in spider threads to the substrate to avoid being swept away by currents adhesives, particularly the ability to stick in wet conditions, provides (Kamino, 2010; Waite, 2017). Like most commercial adhesives, insight in designing synthetic adhesives for biomedical applications. bioadhesives typically have an initial low-viscosity phase, during which they establish surface contact, followed by a phase of KEY WORDS: Adhesive, Biomaterial, Hygroscopic, Prey capture, increased stiffness, which allows them to resist the crack Self-assembling propagation that leads to failure (Gent, 1996). English ivy clings to tree trunks by secreting a low-viscosity adhesive solution that Introduction – spider diversity and the role of prey capture spreads before water evaporates, hardening it into a matrix (Huang thread et al., 2016). However, the challenge is much greater for aquatic Evolution in silk use has played a crucial role in the success of the animals (Stewart et al., 2011). Barnacles and mussels solve the diverse, over 47,000-species-strong arachnid order Araneae to which problem by secreting adhesives that are subsequently enzymatically spiders belong (Vollrath, 2005; Vollrath and Selden, 2007; World hardened (Dickinson et al., 2009; Naldrett, 1993; So et al., 2016; Spider Catalog, 2017). The order Araneae is composed of two Waite, 2017). By contrast, the glycoprotein (see Glossary) glue of suborders: Mesothelae, which have segmented abdomens like an orb-weaving spider’s viscous threads remains hydrated and scorpions and spinnerets that extend from the middle of their pliable in air because it is contained in tiny aquatic spheres (Fig. 1D,E) (Edmonds and Vollrath, 1992; Tillinghast et al., 1993; Townley et al., 1991). This ensures that their glycoprotein adhesive retains its 1Department of Biological Sciences, Virginia Tech, Blacksburg, VA 24061, USA. viscoelasticity for effective adhesion (Sahni et al., 2010). 2Department of Polymer Science, Integrated Bioscience Program, The University of Orb-weaving spiders integrate silk produced from four distinct Akron, Akron, OH 44325, USA. 3Department of Biology, Integrated Bioscience Program, The University of Akron, Akron, OH 44325, USA. silk glands into a highly effective prey capture web (Fig. 1A). Attached by pyriform gland (see Glossary) secretions (Sahni et al., *Author for correspondence ([email protected]) 2012a; Wolff et al., 2015), non-adhesive radial and frame threads B.D.O., 0000-0002-1830-0752; A.D., 0000-0002-3935-7467; T.A.B., 0000-0002- produced by major ampullate glands (see Glossary) absorb and 8166-5981 dissipate the kinetic energy of an insect’s impact (Sensenig et al., Journal of Experimental Biology 1 REVIEW Journal of Experimental Biology (2018) 221, jeb161539. doi:10.1242/jeb.161539 Glossary Young’s modulus Aciniform glands Also referred to as elastic modulus, describes the stiffness of a material, Spinning glands that produce large amounts of silk used to wrap and and is expressed as the energy per cross-sectional area required to immobilize prey. extend a material. Lower values denoting more easily stretched material. Aggregate gland Young’s modulus is determined as the slope of the linear region of a One of two spinning glands that open at the tips of adjacent spigots on material’s stress–strain curve. each posterior lateral spinneret (Fig. 1B) and together coat a flagelliform fiber with a solution of inorganic salts and organic molecules, which are reconfigured to form the outer lipid layer, aqueous layer, glycoprotein core and central granule of a viscous capture thread droplet. 2012), while spirally arrayed, adhesive prey capture threads Aqueous layer produced from flagelliform and aggregate glands (see Glossary) ’ The material that covers a viscous thread s axial lines and adhesive retain the insect (Sahni et al., 2013) until the spider can locate, run to glycoprotein cores. This solution contains the low molecular mass compounds and inorganic salts that confer thread hygroscopicity and and begin to subdue it. Material invested in non-adhesive threads condition and solvate the glycoproteins in the core of a viscous droplet. influences the size and velocity of insects that a web can stop This layer is composed of aggregate gland material that remains after the (Sensenig et al., 2012), and material invested in capture thread glycoprotein cores of droplets are formed. affects the time an insect is trapped (Opell et al., 2017). A retention Axial lines or axial fiber time (see Glossary) difference of even a few seconds can be the One of two protein strands that is spun from a flagelliform gland spigot on difference between a prey being captured or lost (Eberhard, 1989). each posterior lateral spinneret and serves as one of the central support lines of a viscous capture thread. Orb-weaving spiders are not unique in relying on extended Cribellate thread phenotypes (see Glossary) for important functions (Dawkins, Plesiomorphic type of dry prey capture thread comprising an outer layer 1982), nor are they the only animals that use these products for of thousands of nanofibrils that surround larger supporting fibers. prey capture. For example, parchment worms and caddisfly larvae Extended phenotype employ nets to filter organic material from the water (Flood and A physical product or construction of an animal that is genetically Fiala-Médioni, 1982; Mackay and Wiggins, 1979). Like other determined, affects its fitness and, therefore, can be shaped by natural extended phenotypes (see Glossary), orb spider threads and webs selection. Flagelliform gland exhibit physical and architectural plasticity (Blamires, 2010; A spinning gland that opens at the tip of a spigot found on each of the Blamires et al., 2014, 2016, 2017; Crews and Opell,
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