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| Amino acid composition of the major ampullate silk of Orbiculariae spiders compared to Fecenia. All values are mean percent- age of the total of all amino acids
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Correlated evolution of traits can act synergistically to facilitate organism function. But, what happens when constraints exist on the evolvability of some traits, but not others? The orb web was a key innovation in the origin of >12,000 species of spiders. Orb evolution hinged upon the origin of novel spinning behaviors and innovations in silk ma...
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... nests deep within the RTA clade ( Fig. 2; see also 29 ). We found that Fecenia's major ampullate silk is both tougher and stronger than major ampullate silk produced by its RTA clade rela- tives (toughness and true stress respectively in Fig. 3 and Table S1; P 5 0.0001 in post-hoc comparisons for both parameters). This sup- ports the hypothesis that the evolution of aerial web-spinning beha- viors is accompanied by strong selection on silk biomaterial properties in spiders. ...
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... sup- ports the hypothesis that the evolution of aerial web-spinning beha- viors is accompanied by strong selection on silk biomaterial properties in spiders. However, Fecenia's silk resembles that of its phylogenetic relatives in RTA clade in being both stiff and non- extensible (Young's modulus and true strain respectively in Fig. 3 and Table S1; P 5 0.15 and P 5 0.051 respectively in post-hoc comparisons). Table 1 compares the amino acid composition of major ampullate silk from Fecenia webs to published compositions for a variety of Orbiculariae, including Latrodectus which spins an evolutionarily derived three-dimensional cobweb. ...
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... Fecenia's silk resembles that of its phylogenetic relatives in RTA clade in being both stiff and non- extensible (Young's modulus and true strain respectively in Fig. 3 and Table S1; P 5 0.15 and P 5 0.051 respectively in post-hoc comparisons). Table 1 compares the amino acid composition of major ampullate silk from Fecenia webs to published compositions for a variety of Orbiculariae, including Latrodectus which spins an evolutionarily derived three-dimensional cobweb. Fecenia major ampullate silk contains (mean 6 SD) 3.3 6 0.3% proline. ...
Citations
... One potential mechanism driving this pattern is an increase in the proportion of MaSp2 proteins in dragline silk. Surveys of spidroin amino acid motif representation throughout spiders [12,23,[42][43][44] indicate that dragline silk in basal Araneomorphae taxa have sequence characteristics more similar to MaSp1 and that the GPGXX and QQ motifs found in MaSp2 arose later in spider evolution. While spiders from the retrolateral tibial apophysis (RTA) clade, Uloboridae, Theridiidae, and Nephilinae all exhibit some evidence of MaSp2 expression, derived Araneidae spiders have substantially increased their investment in this silk protein. ...
... While spiders from the retrolateral tibial apophysis (RTA) clade, Uloboridae, Theridiidae, and Nephilinae all exhibit some evidence of MaSp2 expression, derived Araneidae spiders have substantially increased their investment in this silk protein. These orb-weavers exhibit the highest proportion of proline in dragline silk which reflects an increased use of MaSp2 and likely contributes to the enhanced extensibility of dragline fibers in this group [26,28,29,42]. ...
... While selection for increased gene expression may drive the initial fixation of duplicate gene copies, the long-term maintenance and divergence of paralogs imply shifts in the functional roles of these genes. The functional differences between MaSp1 and MaSp2 are well established [18,30,62] and the increased use of MaSp2 is critical to the evolutionary success of orb-weavers [2,42,84]. Additional MaSp genes that likely impact fiber performance, such as MaSp3, have arisen within the Araneidae [50,52,55]. ...
The evolutionary diversification of orb-web weaving spiders is closely tied to the mechanical performance of dragline silk. This proteinaceous fiber provides the primary structural framework of orb web architecture, and its extraordinary toughness allows these structures to absorb the high energy of aerial prey impact. The dominant model of dragline silk molecular structure involves the combined function of two highly repetitive, spider-specific, silk genes (spidroins)—MaSp1 and MaSp2. Recent genomic studies, however, have suggested this framework is overly simplistic, and our understanding of how MaSp genes evolve is limited. Here we present a comprehensive analysis of MaSp structural and evolutionary diversity across species of Argiope (garden spiders). This genomic analysis reveals the largest catalog of MaSp genes found in any spider, driven largely by an expansion of MaSp2 genes. The rapid diversification of Argiope MaSp genes, located primarily in a single genomic cluster, is associated with profound changes in silk gene structure. MaSp2 genes, in particular, have evolved complex hierarchically organized repeat units (ensemble repeats) delineated by novel introns that exhibit remarkable evolutionary dynamics. These repetitive introns have arisen independently within the genus, are highly homogenized within a gene, but diverge rapidly between genes. In some cases, these iterated introns are organized in an alternating structure in which every other intron is nearly identical in sequence. We hypothesize that this intron structure has evolved to facilitate homogenization of the coding sequence. We also find evidence of intergenic gene conversion and identify a more diverse array of stereotypical amino acid repeats than previously recognized. Overall, the extreme diversification found among MaSp genes requires changes in the structure-function model of dragline silk performance that focuses on the differential use and interaction among various MaSp paralogs as well as the impact of ensemble repeat structure and different amino acid motifs on mechanical behavior.
... Silk and webs have featured prominently in studies of spider evolution (e.g., 15,16,18,20,38,48,49,65,99,100). While all spiders produce several types of silk (135), some of these silk types and their associated proteins and genetic machinery are restricted to specific lineages (e.g., 25,31,126). ...
Spiders (Araneae) make up a remarkably diverse lineage of predators that have successfully colonized most terrestrial ecosystems. All spiders produce silk, and many species use it to build capture webs with an extraordinary diversity of forms. Spider diversity is distributed in a highly uneven fashion across lineages. This strong imbalance in species richness has led to several causal hypotheses, such as codiversification with insects, key innovations in silk structure and web architecture, and loss of foraging webs. Recent advances in spider phylogenetics have allowed testing some of these hypotheses, but results are often contradictory, highlighting the need to consider additional drivers of spider diversification. The spatial and historical patterns of diversity and diversification remain contentious. Comparative analyses of spider diversification will advance only if we continue to make progress with studies of species diversity, distribution, and phenotypic traits, together with finer-scale phylogenies and genomic data.
Expected final online publication date for the Annual Review of Entomology, Volume 66 is January 11, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... Diese Entwicklung wurde dabei von signifikanten Veränderungen in den Genen begleitet, die für MA-Seidenproteine kodieren. Zudem wurde die hohe Zähigkeit der MA-Seide rad netzbauender Spinnen erst nach der Evolution eines zweiten Proteins MaSp2 ermöglicht, welches die Elastizität der Seide enorm verbesserte [10,11]. Die Angaben, wann MA-Seide während der Spinnen evolution auftrat, variieren, da unterschiedliche phylo genetische Rekonstruktionen ver schiedene Zeitpunkte für die Aufspaltung in araneomorphe und mygalomorphe Spinnen angeben [5]. ...
... Bei Arten, die sekundär das Netz als Fangstrategie aufgegeben haben und deren Seiden damit keinem evolutio närem Druck zum Einfangen von Beutetieren ausgesetzt sind, existiert zudem ein Trend zu Spinnenseiden mit besonders geringer Festigkeit und Zähigkeit [13]. Umgekehrt weisen die Seiden von Spinnen, die so genannte "Pseudo-Radnetze" weben, aber systematisch nicht zur Gruppe der Echten Radnetzspinnen gehören, ähnlich hohe Zugfestigkeiten auf wie Netze von Spinnen der Radnetz-Gruppe [11]. Dies deutet darauf hin, dass unabhängig von der verwendeten Seide die zugrunde liegenden evolutionären Drücke bezüglich mecha nischer Eigenschaften gleich sind. ...
Zusammenfassung
Der evolutionäre Erfolg von Spinnen (Araneae) ist eng mit der Entwicklung und vielfältigen Verwendung ihrer Spinnenseiden verknüpft. Das Fasermaterial wird z. B. zum Schutz der Nachkommen, zur Verbreitung und Orientierung, und für den Beutefang genutzt. Etwa die Hälfte der über 48.000 bekannten Arten baut Netze, deren Variabilität als Beispiel für eine Koevolution mit Insekten und deren Lebensräumen gilt. Im Laufe der Evolution entstanden durch Anpassungen an die Beuteökologie und Veränderungen der Spidroine auf molekularer Ebene Hochleistungsmaterialien wie die Seiden der Großen Ampullendrüse, deren Zähigkeit die vieler technischer Materialien überragt. Die Etablierung einer rekombinanten Produktion von designten Spidroinen im industriellen Maßstab hat die Nutzung biokompatibler, wundheilungsfördernder und bakteriostatischer Seiden als nachhaltige Biopolymere in vielfältigen Anwendungen in Kosmetik, Biomedizin, Spezialtextilien, Filtermaterialien und Nanobiotechnologie ermöglicht.
... The nanofibrils at the outer edges of the thread are responsible for the overall thread stickiness (Opell and Schwend, 2009). The pseudoflagelliform silk is relatively stiff, strong, and inextensible compared to the counterpart flagelliform axial fibres used in the viscous capture threads of the more derived orb weaving spiders (Kohler and Vollrath, 1995;Blackledge et al., 2012). Cribellate threads can, nevertheless, attain high extensibility if the cribellar nanofibril's contribution can extend after the axial fibers have ruptured (Blackledge and Hayashi, 2006b). ...
... While our amino acid composition and gene expression analyses showed that there were differences in MaSp2 expression across the two populations, the MaSp2 expressions found for spiders from both populations were considerably low compared with MaSp1 expressions in both populations (see Fig. 4). The MaSp2 protein is thought to be predominant in the silks of many orb web building spiders 35 (but see Bittencourt et al. 36 ). However, B. longinqua belongs to the distantly related family Desidae 17 . ...
... In our Sydney and Montevideo laboratories we collected silk from each spider on individually constructed 3 mm × 1 mm steel frames with 0.5 mm × 0.5 mm windows 35 . We pulled the silk threads perpendicularly across the frame window and ran the spool for ~2 h at a constant speed, thus ensuring approximately 2000 rounds of silk were wrapped around the frame windows. ...
There are substantive problems associated with invasive species, including threats to endemic organisms and biodiversity. Understanding the mechanisms driving invasions is thus critical. Variable extended phenotypes may enable animals to invade into novel environments. We explored here the proposition that silk variability is a facilitator of invasive success for the highly invasive Australian house spider, Badumna longinqua. We compared the physico-chemical and mechanical properties and underlying gene expressions of its major ampullate (MA) silk between a native Sydney population and an invasive counterpart from Montevideo, Uruguay. We found that while differential gene expressions might explain the differences in silk amino acid compositions and protein nanostructures, we did not find any significant differences in silk mechanical properties across the populations. Our results accordingly suggest that B. longinqua’s silk remains functionally robust despite underlying physico-chemical and genetic variability as the spider expands its range across continents. They also imply that a combination of silk physico-chemical plasticity combined with mechanical robustness might contribute more broadly to spider invasibilities.
... Our understanding of the covariations between spider web building and silk properties is an interesting case in point. Broad phylogenetic studies across the major spider groups have shown that spiders that build webs produce the toughest and most extensible major ampullate (MA) silks (Sensenig et al., 2010;Blackledge et al., 2012;Cranford et al., 2014). However, spider webs and their silks are both highly plastic, that is they vary significantly within individual spiders across environments (Boutry & Blamires, 2013;Blamires et al., 2017a). ...
... Phylogenetic analyses have revealed that the MA silks of web-building Araneoidea have the greatest elasticity and toughness (Swanson et al., 2006a,b;Sensenig et al., 2010). The presence of MaSp2-type proteins has thus far only been reported for the silks of orb-web-building spiders (Orbiculariae clade) (Gatesy et al., 2001;Garb et al., 2006;Bittencourt et al., 2010;Blackledge et al., 2012) and is thought to be important for facilitating MA silk elasticity and toughness within webs (Hayashi et al., 1999;Garb et al., 2006;Blackledge et al., 2012). It may accordingly be expected that enhanced MA silk extensibility and toughness is necessary for spider webs to effectively capture flying or falling prey. ...
... Phylogenetic analyses have revealed that the MA silks of web-building Araneoidea have the greatest elasticity and toughness (Swanson et al., 2006a,b;Sensenig et al., 2010). The presence of MaSp2-type proteins has thus far only been reported for the silks of orb-web-building spiders (Orbiculariae clade) (Gatesy et al., 2001;Garb et al., 2006;Bittencourt et al., 2010;Blackledge et al., 2012) and is thought to be important for facilitating MA silk elasticity and toughness within webs (Hayashi et al., 1999;Garb et al., 2006;Blackledge et al., 2012). It may accordingly be expected that enhanced MA silk extensibility and toughness is necessary for spider webs to effectively capture flying or falling prey. ...
While phylogenetic studies have shown covariation between the properties of spider major ampullate (MA) silk and web building, both spider webs and silks are highly plastic so we cannot be sure whether these traits functionally co‐vary or just vary across environments that the spiders occupy. Since MaSp2‐like proteins provide MA silk with greater extensibility, their presence is considered necessary for spider webs to effectively capture prey. Wolf spiders (Lycosidae) are predominantly non‐web building, but a select few species build webs. We accordingly collected MA silk from two web building and six non‐web building species found in semi‐rural ecosystems in Uruguay to test whether the presence of MaSp2‐like proteins (indicated by amino acid composition), silk mechanical properties, and silk nanostructures, were associated with web building across the group. The web building and non‐web building species were from disparate subfamilies so we estimated a genetic phylogeny to perform appropriate comparisons. For all of the properties measured we found differences between web building and non‐web building species. A phylogenetic regression model confirmed that web building and not phylogenetic inertia influences silk properties. Our study definitively showed an ecological influence over spider silk properties. We expect that the presence of the MaSp2‐like proteins and the subsequent nanostructures improves the mechanical performance of silks within the webs. Our study furthers our understanding of spider web and silk co‐evolution and the ecological implications of spider silk properties.
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... For the vast majority of orb weavers, the origin of this web design is ancient and probably singular, but in the case of Fecenia, a small genus in the family Psechridae, the orb web has evolved more recently and independently from within a large clade of mostly cursorial and ground sheet weaving spiders (Agnarsson et al., 2013;Blackledge et al., 2012a;Levi, 1982). This remarkable case of convergence ( Fig. 1) offers an ideal opportunity to study how silk proteins, web-building behaviors, and anatomy coevolve to recreate this remarkable snare. ...
... Getting the phylogeny wrong can mislead us in how we infer the evolution of traits. For example, prior research argued that Fecenia silks could never fully match the properties of true orb weavers because, as recently as five years ago, it was assumed that true orb weavers originated separately (Fig. 2 Left), and that this group uniquely and exclusively acquired a key silk protein called major ampullate spidroin 2 (MaSp2) (Blackledge et al., 2012a;Blackledge et al., 2012b). MaSp2 is rich in proline residues that are thought to disrupt intermolecular bonds resulting in high extensibility and supercontraction (Gatesy et al., 2001;Hayashi and Lewis, 1998). ...
... While superfamily relationships deep within the spider tree have greatly improved though phylogenomics, well-supported phylogenies of lycosoid spiders continue to elude us. Five recent papers that address these relationships using traditional molecular markers (Agnarsson et al., 2013;Bayer and Schonhofer, 2013;Blackledge et al., 2012a;Moradmand et al., 2014;Wheeler et al., 2016), each arrive at a different set of relationships (Fig. 3), and all but one fail to support monophyly of the Psechridae. Consistent with some older morphological studies (Davila, 2003;Griswold, 1993), these results tend to group psechrids closer to true wolf spiders (Lycosidae) rather than tropical wolf spiders (Ctenidae). ...
Psechrids are an enigmatic family of S.E. Asian spiders. This small family builds sheet webs and even orb webs, yet unlike other orb weavers, its putative relatives are largely cursorial lycosoids - a superfamily of approximately seven spider families related to wolf spiders. The orb web was invented at least twice: first in a very ancient event, and then second, within this clade of wolf-like spiders that reinvented this ability. Exactly how the spiders modified their silks, anatomy, and behaviors to accomplish this transition requires that we identify their precise evolutionary origins -- yet, thus far, molecular phylogenies show poor support and considerable disagreement. Using phylogenomic methods based on whole body transcriptomes for psechrids and their putative relatives, we have recovered a well-supported phylogeny that places the Psechridae sister to the Ctenidae -- a family of mostly cursorial habits but that, as with all psechrids, retains some cribellate species. Although this position reinforces the prevailing view that orb weaving in psechrids is largely a consequence of convergence, it is still possible some components of this behavior are retained or resurrected in common with more distant true orb weaving ancestors.
... However, among some webless spiders (e.g. D. tenebrosus, P. viridans), the absence of MaSp2 data might reflect actual expression patterns, as has been proposed [45,46]. The accession codes for sequences used in the study are given in S1 Table along with other details. ...
... Since web architecture reflects prey capture strategy and thus implies certain demands on fiber performance (e.g. aerial orb webs are designed to catch flying insects, reflected in the exceptional toughness values of the component dragline fibers [45,55], the results of the analysis support the hypothesis that the abundance of the MaSp2 motifs GP, QQ, and GGY play a role in modulating the mechanical properties of dragline silk. ...
The extraordinary mechanical properties of spider dragline silk are dependent on the highly repetitive sequences of the component proteins, major ampullate spidroin 1 and 2 (MaSp2 and MaSp2). MaSp sequences are dominated by repetitive modules composed of short amino acid motifs; however, the patterns of motif conservation through evolution and their relevance to silk characteristics are not well understood. We performed a systematic analysis of MaSp sequences encompassing infraorder Araneomorphae based on the conservation of explicitly defined motifs, with the aim of elucidating the essential elements of MaSp1 and MaSp2. The results show that the GGY motif is nearly ubiquitous in the two types of MaSp, while MaSp2 is invariably associated with GP and di-glutamine (QQ) motifs. Further analysis revealed an extended MaSp2 consensus sequence in family Araneidae, with implications for the classification of the archetypal spidroins ADF3 and ADF4. Additionally, the analysis of RNA-seq data showed the expression of a set of distinct MaSp-like variants in genus Tetragnatha. Finally, an apparent association was uncovered between web architecture and the abundance of GP, QQ, and GGY motifs in MaSp2, which suggests a co-expansion of these motifs in response to the evolution of spiders' prey capture strategy.
... Detailed studies have established the links between the expression of certain spider silk genes and the proteins (spidroins) produced [54][55][56][57][58][59][60]. The properties of the silks are described across species, so we know that: (i) the spidroins form crystalline and non-crystalline nanostructures that respectively contribute to the silk's strength and extensibility [54][55][56][57], and; (ii) the amino acid composition of the spidroins correlates well with certain nanostructures [54,[59][60][61][62]. Dragline silk is manufactured in the major ampullate gland, which consists of three subsections that serve spidroin production, storage of the liquid precursor (dope) and fibre formation respectively (figure 2(a)). ...
... Detailed studies have established the links between the expression of certain spider silk genes and the proteins (spidroins) produced [54][55][56][57][58][59][60]. The properties of the silks are described across species, so we know that: (i) the spidroins form crystalline and non-crystalline nanostructures that respectively contribute to the silk's strength and extensibility [54][55][56][57], and; (ii) the amino acid composition of the spidroins correlates well with certain nanostructures [54,[59][60][61][62]. Dragline silk is manufactured in the major ampullate gland, which consists of three subsections that serve spidroin production, storage of the liquid precursor (dope) and fibre formation respectively (figure 2(a)). Prior to extrusion the dope flows through a funnelshaped aperture [63], and the decreased lumen width generates shear stress on the dope, inducing a thinning and solidification of the fibre [64]. ...
Biomimetics, the transfer of functional principles from living systems into product designs, is increasingly being utilized by engineers. Nevertheless, recurring problems must be overcome if it is to avoid becoming a short-lived fad. Here we assess the efficiency and suitability of methods typically employed by examining three flagship examples of biomimetic design approaches from different disciplines: (1) the creation of gecko-inspired adhesives; (2) the synthesis of spider silk, and (3) the derivation of computer algorithms from natural self-organizing systems. We find that identification of the elemental working principles is the most crucial step in the biomimetic design process. It bears the highest risk of failure (e.g. losing the target function) due to false assumptions about the working principle. Common problems that hamper successful implementation are: (i) a discrepancy between biological functions and the desired properties of the product, (ii) uncertainty about objectives and applications, (iii) inherent limits in methodologies, and (iv) false assumptions about the biology of the models. Projects that aim for multi-functional products are particularly challenging to accomplish. We suggest a simplification, modularisation and specification of objectives, and a critical assessment of the suitability of the model. Comparative analyses, experimental manipulation, and numerical simulations followed by tests of artificial models have led to the successful extraction of working principles. A searchable database of biological systems would optimize the choice of a model system in top-down approaches that start at an engineering problem. Only when biomimetic projects become more predictable will there be wider acceptance of biomimetics as an innovative problem-solving tool among engineers and industry.
... Spiders have evolved multiple silk glands that produce fibres and glues with different mechanical properties for specific needs [2,[4][5][6][7]. It has frequently been proposed that the high performance of dragline silk and thread coating glues has facilitated the evolution of economic aerial traps that are effective at intercepting flying insects [8][9][10][11]. The individual silk fibres in spider webs are attached either to each other or to the substrate. Presumably, the strength of the attachment is concomitant with the strength of the attached fibre. ...
Building behaviour in animals extends biological functions beyond bodies. Many studies have emphasized the role of behavioural programmes, physiology and extrinsic factors for the structure and function of buildings.
Structure attachments associated with animal constructions offer yet unrealized research opportunities. Spiders build a variety of one- to three-dimensional structures from silk fibres. The evolution of economic web shapes as a key for ecological success in spiders has been related to the emergence of high performance silks and thread coating glues. However, the role of thread anchorages has been widely neglected in those models. Here, we show that orb-web (Araneidae) and hunting spiders (Sparassidae) use different silk application patterns that determine the structure and robustness of the joint in silk thread anchorages. Silk anchorages of orb-web spiders show a greater robustness against different loading situations, whereas the silk
anchorages of hunting spiders have their highest pull-off resistance when loaded parallel to the substrate along the direction of dragline spinning. This suggests that the behavioural ‘printing’ of silk into attachment discs
along with spinneret morphology was a prerequisite for the evolution of extended silk use in a three-dimensional space. This highlights the ecological role of attachments in the evolution of animal architectures.
