Intragenic homogenization and multiple copies of prey-wrapping silk genes in Argiope garden spiders.

BackgroundSpider silks are spectacular examples of phenotypic diversity arising from adaptive molecular evolution. An individual spider can produce an array of specialized silks, with the majority of constituent silk proteins encoded by members of the spidroin gene family. Spidroins are dominated by tandem repeats flanked by short, non-repetitive N- and C-terminal coding regions. The remarkable mechanical properties of spider silks have been largely attributed to the repeat sequences. However, the molecular evolutionary processes acting on spidroin terminal and repetitive regions remain unclear due to a paucity of complete gene sequences and sampling of genetic variation among individuals. To better understand spider silk evolution, we characterize a complete aciniform spidroin gene from an Argiope orb-weaving spider and survey aciniform gene fragments from congeneric individuals.ResultsWe present the complete aciniform spidroin (AcSp1) gene from the silver garden spider Argiope argentata (Aar_AcSp1), and document multiple AcSp1 loci in individual genomes of A. argentata and the congeneric A. trifasciata and A. aurantia. We find that Aar_AcSp1 repeats have >98% pairwise nucleotide identity. By comparing AcSp1 repeat amino acid sequences between Argiope species and with other genera, we identify regions of conservation over vast amounts of evolutionary time. Through a PCR survey of individual A. argentata, A. trifasciata, and A. aurantia genomes, we ascertain that AcSp1 repeats show limited variation between species whereas terminal regions are more divergent. We also find that average dN/dS across codons in the N-terminal, repetitive, and C-terminal encoding regions indicate purifying selection that is strongest in the N-terminal region.ConclusionsUsing the complete A. argentata AcSp1 gene and spidroin genetic variation between individuals, this study clarifies some of the molecular evolutionary processes underlying the spectacular mechanical attributes of aciniform silk. It is likely that intragenic concerted evolution and functional constraints on A. argentata AcSp1 repeats result in extreme repeat homogeneity. The maintenance of multiple AcSp1 encoding loci in Argiope genomes supports the hypothesis that Argiope spiders require rapid and efficient protein production to support their prolific use of aciniform silk for prey-wrapping and web-decorating. In addition, multiple gene copies may represent the early stages of spidroin diversification

Eight Legged Encounters

This program was funded in part by a National Science Foundation grant (DRL–1241482 to EAH). Material was developed in collaboration with Marie- Claire Chelini, Jessie Rose Storz, Cody Storz, and Malcolm Rosenthal. Steven Schwartz, Jason Stafstrom, Kathy French, Priscilla Grew, and Judy Diamond were all extremely helpful in grant writing, facilitating the first live event, and/or discussions. Pawl Tisdale (artist) was phenomenal to work with on all aspects of the project! TABLE OF CONTENTS CLASSIFICATION & TAXONOMY STATIONS I. WHAT IS AN ARTHROPOD? page 4 a. The goal of this station is to introduce the audience to some basic information about “arthropods”. Who are they? How and why are they grouped together? Answers to these questions are achieved through a sorting game with plastic animals. II. CREATE A CHELICERATE page 14 a. This station introduces the audience to the basic characteristics of chelicerates (a group which they have learned about from Station I) by allowing them to build their own chelicerate out of clay. III. ASSEMBLE AN ARACHNID page 16 a. Arachnids are surprisingly diverse, with 11 different living orders! This station introduces the audience to the diversity of body types found within the 11 living arachnid orders through a coloring activity. SPIDER-SPECIFIC STATIONS (ORDER ARANEAE) IV. BUILD A BURROW page 20 a. The first spiders didn’t build orb webs to catch prey out of the air, but instead, built silk-lined burrows with trapdoors. This station explores the early function of spider silk. V. CRIBELLATE VS. ECRIBELLATE SILK page 22 a. Spiders have evolved two different ways to improve the efficiency of prey capture with their webs. This station explores those two evolutionary solutions. VI. WEAVE A WEB page 24 a. Orb webs (the classical web most non-biologists envision when asked to think of a spider web) are quite complex structures. How do spiders build orb webs? Do they use the same type of silk for the entire web? Answers to these questions can be obtained as participants are guided through their own web-weaving exercise. VII. CATCH A MOTH page 27 a. This station highlights the unique foraging strategy of the ‘bolas spider’ through a game in which participants try to catch a moth out of the air using a lasso. VIII. TISSUE PAPER FLOWER page 29 a. This station lets the audience create their own tissue paper flower upon which their chosen crab spider (made of paper) can forage. It introduces the fact that some spiders can change color and highlights the adaptive value of camouflage. RESEARCH-RELATED STATIONS IX. MICROSCOPE MADNESS page 33 a. This station provides the audience an opportunity to take an up-close look at spiders - to examine body parts they cannot normally see and to get them thinking about how these details might relate to an animals’ lifestyle or evolutionary history. X. COMMUNITY EXPERIMENT page 38 a. This station engages participants in a hand’s on spider feeding experiment that examines the influence of seismic (vibratory) cues on foraging success. Participants are encouraged to imagine how their results may relate to the evolution of courtship displays that incorporate specific sensory modalities. MISCELANEOUS STATIONSXI. SILKEN SPINNERS page 44 a. This station provides some “down time” for participants, where they can sit and watch the amazing footage and associated information put together by the BBC in David Attenborough’s “Silken Spinners” episode from Life in the Undergrowth.XII. SOUND STATION page 45 a. Most people do not realize that some spiders can “sing” in the form of stereotyped vibrations that are sent through a substrate, or surface upon which they are standing (e.g. a leaf, a twig, a blade of grass, etc.). Here, participants can listen to the sounds of spiders and are asked to imagine if they might find these songs attractive. XIII. SPIDER DANCE DISCO page 46 a. Not only can spiders sing, but they can also dance! Participants can observe some of the amazing dances that spiders do and can learn some of their own spider dance moves by watching the “Spider Dance Disco” XIV. READ ALOUD page 47 a. This station enables participants to play with some arachnid stuffed animals, puzzles, and to look through arachnid-related children’s books. Several books are listed as suggestions for read alouds. PATH OF PREDATORS XV. LIVING ARACHNID ORDERS page 48 a. Araneae, Amblypygi, Thelyphonida, Schizomida, Scorpiones, Solifugae, Palpigradi, Ricinulei, Pseudoscorpiones, Acari, Opilione

Prey localization in spider orb webs using modal vibration analysis

Spider webs are finely tuned multifunctional structures, widely studied for their prey capture functionalities such as impact strength and stickiness. However, they are also sophisticated sensing tools that enable the spider to precisely determine the location of impact and capture the prey before it escapes. In this paper, we suggest a new mechanism for this detection process, based on potential modal analysis capabilities of the spider, using its legs as distinct distributed point sensors. To do this, we consider a numerical model of the web structure, including asymmetry in the design, prestress, and geometrical nonlinearity effects. We show how vibration signals deriving from impacts can be decomposed into web eigenmode components, through which the spider can efficiently trace the source location. Based on this numerical analysis, we discuss the role of the web structure, asymmetry, and prestress in the imaging mechanism, confirming the role of the latter in tuning the web response to achieve an efficient prey detection instrument. The results can be relevant for efficient distributed impact sensing applications

Orb-weaver Diversity and Niche Partitioning in Ecuador’s Amazonian Foothills: What spiders can reveal about tree fall gaps, streams, and cultivated areas

As abundant predators at the top of arthropod food chains, spiders are excellent bioindicators. Araneae is a megadiverse and extremely understudied order, especially in the tropics. This study aims to investigate the diversity of orb-weaver spiders across a disturbance gradient and variety of habitat types as well as their microhabitat preferences and potential niche partitioning. Spider collection was performed on spiders of the families Araneidae, Tetragnathidae, and Theridiosomatidae in Sumak Kawsay in Situ biological reserve in the lower elevation cloud forest of Ecuador’s Andean foothills. Spiders and webs were observed and analyzed from primary and secondary forest tree fall gaps, stream corridors in primary and secondary forests, and open areas in cultivated land around the lodge. In general, orb-weaver diversity decreased from primary to secondary to cultivated habitat and there was very little species overlap between forested sites and cultivated sites. The family distributions varied between the habitat types: tree gaps, streams, and cultivated open areas. No dependence was found between various ecological variables within the samples. However, the relative abundance of different morphospecies across height strata demonstrated separate niches were occupied by different species. Additionally, the height strata where webs were found varied with the microhabitat and vegetative qualities present in the different habitat types. With an increase in microhabitat complexity, there was an increase in available niches and thus in orb-weaver diversity

Extended spider cognition

HFJ received a visiting professor fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - Brazil) (PDE PDE232691/2014-2). Research supported in part by a Grant from the John Templeton Foundation to KNL.There is a tension between the conception of cognition as a central nervous system (CNS) process, and a view of cognition as extending towards the body or the contiguous environment. The centralised conception requires large or complex nervous systems to cope with complex environments. Conversely, the extended conception involves the outsourcing of information processing to the body or environment, thus making fewer demands on the processing power of the CNS. The evolution of extended cognition should be particularly favoured among small, generalist predators such as spiders, and here we review the literature to evaluate the fit of empirical data with these contrasting models of cognition. Spiders do not seem to be cognitively limited, displaying a large diversity of learning processes, from habituation to contextual learning, including a sense of numerosity. To tease apart the central from the extended cognition, we apply the mutual manipulability criterion, testing the existence of reciprocal causal links between the putative elements of the system. We conclude that the web threads and configurations are integral parts of the cognitive systems. The extension of cognition to the web helps to explain some puzzling features of spider behaviour and seems to promote evolvability within the group, enhancing innovation through cognitive connectivity to variable habitat features. Graded changes in relative brain size could also be explained by outsourcing information processing to environmental features. More generally, niche-constructed structures emerge as prime candidates for extending animal cognition, generating the selective pressures that help to shape the evolving cognitive system.Publisher PDFPeer reviewe

Spider webs capture environmental DNA from terrestrial vertebrates

Environmental DNA holds significant promise as a non-invasive tool for tracking terrestrial biodiversity. However, in non-homogenous terrestrial environments, the continual exploration of new substrates is crucial. Here we test the hypothesis that spider webs can act as passive biofilters, capturing eDNA from vertebrates present in the local environment. Using a metabarcoding approach, we detected verte brate eDNA from all analyzed spider webs (N = 49). Spider webs obtained from an Australian woodland locality yielded vertebrate eDNA from 32 different species, including native mammals and birds. In contrast, webs from Perth Zoo, less than 50 km away, yielded eDNA from 61 different vertebrates and produced a highly distinct species composition, largely reflecting exotic species hosted in the zoo. We show that higher animal biomass and proximity to animal enclosures increased eDNA detection probabil ity in the zoo. Our results indicate a tremendous potential for using spider webs as a cost-effective means to monitor terrestrial vertebrates

Blueprint for a high-performance biomaterial: full-length spider dragline silk genes.

Spider dragline (major ampullate) silk outperforms virtually all other natural and manmade materials in terms of tensile strength and toughness. For this reason, the mass-production of artificial spider silks through transgenic technologies has been a major goal of biomimetics research. Although all known arthropod silk proteins are extremely large (>200 kiloDaltons), recombinant spider silks have been designed from short and incomplete cDNAs, the only available sequences. Here we describe the first full-length spider silk gene sequences and their flanking regions. These genes encode the MaSp1 and MaSp2 proteins that compose the black widow's high-performance dragline silk. Each gene includes a single enormous exon (>9000 base pairs) that translates into a highly repetitive polypeptide. Patterns of variation among sequence repeats at the amino acid and nucleotide levels indicate that the interaction of selection, intergenic recombination, and intragenic recombination governs the evolution of these highly unusual, modular proteins. Phylogenetic footprinting revealed putative regulatory elements in non-coding flanking sequences. Conservation of both upstream and downstream flanking sequences was especially striking between the two paralogous black widow major ampullate silk genes. Because these genes are co-expressed within the same silk gland, there may have been selection for similarity in regulatory regions. Our new data provide complete templates for synthesis of recombinant silk proteins that significantly improve the degree to which artificial silks mimic natural spider dragline fibers

A Meal or a Male: The ‘Whispers’ Of Black Widow Males Do Not Trigger a Predatory Response in Females

Introduction Female spiders are fine-tuned to detect and quickly respond to prey vibrations, presenting a challenge to courting males who must attract a female’s attention but not be mistaken for prey. This is likely particularly important at the onset of courtship when a male enters a female’s web. In web-dwelling spiders, little is known about how males solve this conundrum, or about their courtship signals. Here we used laser Doppler vibrometry to study the vibrations produced by males and prey (house flies and crickets) on tangle webs of the western black widow Latrodectus hesperus and on sheet webs of the hobo spider Tegenaria agrestis. We recorded the vibrations at the location typically occupied by a hunting female spider. We compared the vibrations produced by males and prey in terms of their waveform, dominant frequency, frequency bandwidth, amplitude and duration. We also played back recorded male and prey vibrations through the webs of female L. hesperus to determine the vibratory parameters that trigger a predatory response in females. Results We found overlap in waveform between male and prey vibrations in both L. hesperus and T. agrestis. In both species, male vibrations were continuous, of long duration (on average 6.35 s for T. agrestis and 9.31 s for L. hesperus), and lacked complex temporal patterning such as repeated motifs or syllables. Prey vibrations were shorter (1.38 - 2.59 s), sporadic and often percussive. Based on the parameters measured, courtship signals of male L. hesperus differed more markedly from prey cues than did those of T. agrestis. Courtship vibrations of L. hesperus males differed from prey vibrations in terms of dominant frequency, amplitude and duration. Vibrations of T. agrestis males differed from prey in terms of duration only. During a playback experiment, L. hesperus females did not respond aggressively to low-amplitude vibrations irrespective of whether the playback recording was from a prey or a male. Conclusions Unlike courtship signals of other spider species, the courtship signals of L. hesperus and T. agrestis males do not have complex temporal patterning. The low-amplitude ‘whispers’ of L. hesperus males at the onset of courtship are less likely to trigger a predatory response in females than the high-amplitude vibrations of struggling prey

Selective Utilization of Microhabitats by Web-building Spiders

Natural enemies are members of complex ecological communities, and their ability to contribute to the biological control of pest organisms is strongly influenced by a convoluted network of ecological interactions with many other organisms within these communities. Researchers must develop an understanding of the mechanisms that shape trophic webs to predict and promote top-down effects of predators. The behavior of predators can have a strong influence on their potential as biological control agents. Web-building spiders are a useful example organism for the study of natural enemy behavior because of the experimentally tractable nature of their foraging behavior. Specifically, patterns in microhabitat utilization and web construction by spiders provide insights into foraging behavior and pest-suppression potential. In field collections, spiders were found to utilize microhabitats in a species-specific manner. Molecular gut-content analysis and a mathematical model showed that two spiders belonging to different web-building guilds differed in their dependence on microhabitat-specific prey activity-densities. In particular, the sheet-weaving guild constructed webs in microhabitats with the highest densities of springtails (Collembola). High dependence on this non-pest prey also correlated with evidence of increased intraspecific competition, and implies a potential negative effect of springtails on the consumption of pest insects, such as aphids. In laboratory two-choice assays, sheet-weaving spiders selected microhabitats and constructed webs in a flexible, stepwise manner, which allowed spiders to regulate their investment of silk resources to match the profitability of the microhabitat. Spiders also exhibited prey-specific shifts in foraging behavior, constructing webs in the presence of mobile, non-pest springtails, but utilizing active foraging tactics in the presence of sedentary, pest aphids. However, in factorial no-choice assays, pest-consumption rates were not significantly affected by the presence of non-pest springtails, indicating that prey-specific foraging-mode shifts are compatible with biological control. From these results, it is clear that the flexible foraging behavior of web-building spiders has a strong influence on their roles in ecological communities and their position within food webs. This dissertation highlights the importance of understanding the nuances of natural-enemy behavior for properly assessing and promoting biological control services