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Orb-weaver spiders produce upwards of seven different types of silk, each with unique material properties. We focus on the adhesive within orb-weaving spider webs, aggregate glue silk. These droplets are composed of three main components: water, glycoproteins, and a wide range of low molecular mass compounds (LMMCs). These LMMCs are known to play a crucial role in maintaining the material properties of the glycoproteins, aid in water absorption from the environment, and increase surface adhesion. Orb-weavers within the Cyrtarachninae subfamily are moth specialists and have evolved glue droplets with novel material properties. This study investigated the biochemical composition and diversity of the LMMCs present in the aggregate glue of eight moth-specialist species and compared them with five generalist orb-weavers using nuclear magnetic resonance (NMR) spectroscopy. We hypothesized that the novel drying ability of moth-specialist glue was accompanied by novel LMMCs and lower overall percentages by silk weight of LMMCs. We measured no difference in LMMC weight by the type of prey specialization, but observed novel compositions in the glue of all eight moth-catching species. Further, we quantified the presence of a previously reported but unidentified compound that appears in the glue of all moth specialists. These silks can provide insight into the functions of bioadhesives and inform our own synthetic adhesives. 

Abstract Stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we assemble and describe a chromosome-level genome assembly of the stalk-eyed fly, Teleopsis dalmanni, to elucidate patterns of divergence associated with SR. The genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally and insertionally active TE families. By resequencing pools of SR and ST males using short and long reads, we find widespread differentiation and divergence between XSR and XST associated with multiple nested inversions involving most of the SR haplotype. Examination of genomic coverage and gene expression data revealed seven X-linked genes with elevated expression and coverage in SR males. The most extreme and likely drive candidate involves an XSR-specific expansion of an array of partial copies of JASPer, a gene necessary for maintenance of euchromatin and associated with regulation of TE expression. In addition, we find evidence for rapid protein evolution between XSR and XST for testis expressed and novel genes, that is, either recent duplicates or lacking a Dipteran ortholog, including an X-linked duplicate of maelstrom, which is also involved in TE silencing. Overall, the evidence suggests that this ancient XSR polymorphism has had a variety of impacts on repetitive DNA and its regulation in this species. 

Arthropod silk is vital to the evolutionary success of hundreds of thousands of species. The primary proteins in silks are often encoded by long, repetitive gene sequences. Until recently, sequencing and assembling these complex gene sequences has proven intractable given their repetitive structure. Here, using high-quality long-read sequencing, we show that there is extensive variation—both in terms of length and repeat motif order—between alleles of silk genes within individual arthropods. Further, this variation exists across two deep, independent origins of silk which diverged more than 500 Mya: the insect clade containing caddisflies and butterflies and spiders. This remarkable convergence in previously overlooked patterns of allelic variation across multiple origins of silk suggests common mechanisms for the generation and maintenance of structural protein-coding genes. Future genomic efforts to connect genotypes to phenotypes should account for such allelic variation. 

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. 

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.