Changes in spinning anatomy and thread stickiness associated with the origin of orb-weaving spiders

The cribellum is an oval spinning field whose spigots produce silk fibrils that form the outer surfaces of the primitive prey capture threads found in aerial spider webs. A comparison of the cribella and cribellar capture threads of 13 species of spiders representing seven families (Amaurobiidae, Desidae, Dictynidae, Filistatidae, Neolanidae, Oecobiidae, and Uloboridae) confirms that the stickness of a cribellar thread is directly related to the number of spigots on a spider's cribellum. This comparison also demonstrates that the origin of orb-weaving spiders from ancestors that constructed less highly organized webs was associated with increases in both the weight-specific number of cribellum spigots and the weight-specific stickiness of cribellar prey capture threads. In contrast to other cribellate spiders, the number of cribellum spigots of orb-weaving species of the family Uloboridae scales to spider mass. Thus, the origin of orb-weaving spiders involved not only behavioural changes that stylized and restricted the placement of cribellar threads, but also included morphological changes that increased the stickiness of these capture threads by endowing them with more cribellar fibrils.     

The ontogeny of the spinning apparatus of Tengella perfuga (Araneae: Zoropsidae)

Silk is the most recognizable trait of spiders, and silk use has changed throughout spider evolutionary history. While morphology of the adult silk spigot has been a useful character for systematics, few studies have examined the ontogeny of the spinning apparatus, and none of these included cribellate spiders. Here, we report the first published full ontogeny of the spinning apparatus of a cribellate spider, Tengella perfuga. We found the presence of expected spigots: major ampullate gland and piriform gland spigots on the anterior lateral spinneret, minor ampullate gland and aciniform gland spigots on the posterior median spinneret, and aciniform gland spigots on the posterior lateral spinneret. Females, but not males, possessed cylindrical gland spigots on both the posterior median and lateral spinnerets. Spiderlings did not possess a functioning cribellum until the third instar. The cribellum grew with increasing numbers of spigots, but functionality was lost in adult males. Most intriguingly, second instars possessed a distinct triad of pre‐spigots on the posterior lateral spinneret. From the third instar onward, these structures formed the modified spigot along with two flanking spigots (in females) or formed nubbins (in males). We suggest that the modified spigot serves as the source of axial lines in the cribellate silk produced in T. perfuga. We also compare spigot ontogeny from previous studies of ecribellate spiders. These comparisons warrant further exploration using the recent spider tree of life in a phylogenetic comparative analysis of spigot ontogeny datasets, which could yield evidence for homologous spigots across the Araneomorphae, notably the Araneoidea and the Retrolateral Tibial Apophysis (RTA) clades.     

Rounding up the usual suspects: a standard target‐gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb‐weaving spiders with a new family‐rank classification (Araneae,Araneoidea)

We test the limits of the spider superfamily Araneoidea and reconstruct its interfamilial relationships using standard molecular markers. The taxon sample (363 terminals) comprises for the first time representatives of all araneoid families, including the first molecular data of the family Synaphridae. We use the resulting phylogenetic framework to study web evolution in araneoids. Araneoidea is monophyletic and sister to Nicodamoidea rank. n. Orbiculariae are not monophyletic and also include the RTA clade, Oecobiidae and Hersiliidae. Deinopoidea is paraphyletic with respect to a lineage that includes the RTA clade, Hersiliidae and Oecobiidae. The cribellate orb‐weaving family Uloboridae is monophyletic and is sister group to a lineage that includes the RTA Clade, Hersiliidae and Oecobiidae. The monophyly of most Araneoidea families is well supported, with a few exceptions. Anapidae includes holarchaeids but the family remains diphyletic even if Holarchaea is considered an anapid. The orb‐web is ancient, having evolved by the early Jurassic; a single origin of the orb with multiple “losses” is implied by our analyses. By the late Jurassic, the orb‐web had already been transformed into different architectures, but the ancestors of the RTA clade probably built orb‐webs. We also find further support for a single origin of the cribellum and multiple independent losses. The following taxonomic and nomenclatural changes are proposed: the cribellate and ecribellate nicodamids are grouped in the superfamily Nicodamoidea rank n. (Megadictynidae rank res. and Nicodamidae stat. n. ). Araneoidea includes 17 families with the following changes: Araneidae is re‐circumscribed to include nephilines , Nephilinae rank res., Arkyidae rank n. , Physoglenidae rank n. , Synotaxidae is limited to the genus Synotaxus, Pararchaeidae is a junior synonym of Malkaridae ( syn. n. ), Holarchaeidae of Anapidae ( syn. n. ) and Sinopimoidae of Linyphiidae ( syn. n. ).     

The Convergent Development of Orb-webs in Cribellate and Ecribellate Spiders

Orb-webs are highly developed and can be understood as the besttechnical solution of the problem how to place capture-threadsin the most efficient and economical way. They are built bycribellate and ecribellate spiders. Phylogenetical relationsbetween some families of Cribellate and Ecribellate cannot beignored, but for some important reasons it is difficult to imaginethat on the level of orb-weaving cribellate spiders became ecribellateby reducing the cribellum. Thus, these specialised webs musthave developed on both sides independently and are the resultof a convergent evolution. Steps leading from primitive useof threads for capturing insects to the typical and latter modifiedorb-webs of Cribellate and Ecribellate can be discerned.     

Spiders spinning electrically charged nano-fibres

Most spider threads are on the micrometre and sub-micrometre scale. Yet, there are some spiders that spin true nano-scale fibres such as the cribellate orb spider, Uloborus plumipes. Here, we analyse the highly specialized capture silk-spinning system of this spider and compare it with the silk extrusion systems of the more standard spider dragline threads. The cribellar silk extrusion system consists of tiny, morphologically basic glands each terminating through exceptionally long and narrow ducts in uniquely shaped silk outlets. Depending on spider size, hundreds to thousands of these outlet spigots cover the cribellum, a phylogenetically ancient spinning plate. We present details on the unique functional design of the cribellate gland–duct–spigot system and discuss design requirements for its specialist fibrils. The spinning of fibres on the nano-scale seems to have been facilitated by the evolution of a highly specialist way of direct spinning, which differs from the aqua-melt silk extrusion set-up more typical for other spiders.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

The material cost and stickiness of capture threads and the evolution of orb-weaving spiders

Prey capture threads are essential to the operation of spider orb-webs because they prevent insects that have been intercepted from escaping before a spider can subdue them. The volume of material invested in a web's capture threads is related to spider weight and is the same for primitive orb-weavers that produce cribellar capture thread and modern orb-weavers that produce adhesive capture thread. However, as adhesive capture thread achieves greater stickiness relative to its volume, adhesive orb-webs have a greater total stickiness and, consequently, a greater prey capture potential than cribellate orb-webs. These differences appear to have favoured the transition from cribellate to adhesive capture threads and the success of adhesive orb-weavers, which include 95% of all orb-weaving species. Differences in the thread economy and the total stickiness of webs constructed by spiders of different weights also suggest that adhesive orb-weavers should grow more rapidly and be capable of attaining a larger size than cribellate orb-weavers.     

Economics of spider orb-webs: the benefits of producing adhesive capture thread and of recycling silk

1. The replacement of dry, fuzzy cribellar prey capture thread by viscous, adhesive capture thread was a major event in the evolution of orb-weaving spiders. Over 95% of all orb-weaving species now produce adhesive threads.
2. Adhesive thread achieves its stickiness with a much greater material economy than does cribellar thread.
3. Transformational analyses show that, relative to spider mass, adhesive orb-weavers invest less material per mm of capture thread and produce stickier capture threads than do cribellate orb-weavers.
4. The total cost of producing an orb-web that contains cribellar thread is reduced by 32% when a spider recycles its silk and another 34% when these capture threads are replaced by adhesive threads of equal stickiness.
5. The increased economy with which adhesive capture thread achieves its stickiness may have been an important factor that favoured the origin and success of modern orb-weaving spiders that produce adhesive capture threads.     

Tracing the evolutionary origin of a visual signal: the coincidence of wrap attack and web decorating behaviours in orb web spiders (Araneidae)

The silk decorations that adorn the webs of many orb-web spiders are thought to have a signal function, but the evolution of the decorating behaviour remains unresolved. The decoration signal is maintained apparently because it improves foraging efficiency, through either increased encounter rates with prey or reduced damage to the web. Recent investigations suggest that the decorations may originate in a regulation of the activity of the aciniform silk glands, which produce silk for both decorating the web and wrapping prey. This view predicts a link between decorating behaviour and a preference for restraining prey by wrapping with silk, which is evident among species of Argiope spiders. Here I compare the frequency of the wrap attack behaviour in four species of orb-web spiders that occupy the same habitat, but differ in their silk decorating behaviour: two species, Plebs bradleyi and Gea theridioides, build silk decorations, while the other two, Araneus hamiltoni and Backobourkia brounii do not. Spiders were presented with prey items that varied in the ease with which they could be captured, with houseflies being more easily subdued than house crickets. As predicted, the silk decorating species used wrap attacks significantly more often than non-decorating spiders, irrespective of the prey species. These data support the view that both behaviours are evolutionary linked. I propose that silk decorating originated from the evolution of wrap attacking, and that silken web decorations have later evolved into a signal and are now maintained for that function.     

Copulatory mechanics in the wolf spider Agalenocosa pirity reveals a hidden diversity of locking systems in Lycosidae (Araneae)

Genital traits are among the fastest to evolve, and the processes that drive their evolution are intensively studied. Spiders are characterized by complex genitalia, but the functional role of the different structures during genital coupling is largely unknown. Members of one of the largest spider groups, the retrolateral tibial apophysis (RTA) clade, are characterized by a RTA on the male palp, which is thought to play a crucial role during genital coupling. However, the RTA was lost in several families including the species-rich wolf spiders (Lycosidae) leading to the hypothesis that the genital coupling is achieved by alternative mechanisms. Here, we investigate the genital interactions during copulation in the wolf spider Agalenocosa pirity (Zoicinae) on cryofixed mating pairs using electron, optical and X-ray microscopy and compare our findings with other lycosids and entelegyne spiders. We found an unprecedented coupling mechanism for lycosid spiders involving the palea and a membranous cuticle folding adjacent to the epigynal plate. Additionally, we show an uncommon coupling between the median apophysis and the contralateral genital opening, and confirmed that the terminal apophysis acts as functional conductor, as previously hypothesized for males of Zoicinae. Phylogenetic mapping of RTA indicated that the basal tibial process found in Agalenocosa is a secondary acquisition rather than a modified RTA.     

Sociality in theridiid spiders: repeated origins of an evolutionary dead end

Evolutionary "dead ends" result from traits that are selectively advantageous in the short term but ultimately result in lowered diversification rates of lineages. In spiders, 23 species scattered across eight families share a social system in which individuals live in colonies and cooperate in nest maintenance, prey capture, and brood care. Most of these species are inbred and have highly female-biased sex ratios. Here we show that in Theridiidae this social system originated eight to nine times independently among 11 to 12 species for a remarkable 18 to 19 origins across spiders. In Theridiidae, the origins cluster significantly in one clade marked by a possible preadaptation: extended maternal care. In most derivations, sociality is limited to isolated species: social species are sister to social species only thrice. To examine whether sociality in spiders represents an evolutionary dead end, we develop a test that compares the observed phylogenetic isolation of social species to the simulated evolution of social and non-social clades under equal diversification rates, and find that sociality in Theridiidae is significantly isolated. Because social clades are not in general smaller than their nonsocial sister clades, the "spindly" phylogenetic pattern-many tiny replicate social clades-may be explained by extinction rapid enough that a nonsocial sister group does not have time to diversify while the social lineage remains extant. In this case, this repeated origin and extinction of sociality suggests a conflict between the short-term benefits and long-term costs of inbred sociality. Although benefits of group living may initially outweigh costs of inbreeding (hence the replicate origins), in the long run the subdivision of the populations in relatively small and highly inbred colony lineages may result in higher extinction, thus an evolutionary dead end.     

The biology of Pholcus phalangioides (Araneae, Pholcidae): predatory versatility, araneophagy and aggressive mimicry

Predatory versatility occurs in Pholcus phalangioides (Fuesslin). In addition to building prey-catching space webs, P. phalangioides invades webs of other spiders and feeds on the occupants. It acts as an aggressive mimic by performing specialized vibratory behaviours to which the prey-spider responds as it normally would to its own prey. Prey (spiders and insects) is attacked by wrapping. Prey that trips over lines at the edge of a web of P. phalangioides , but fails to enter the web, is successfully attacked: P. phalangioides leans out of its web to throw silk over the prey, keeping as few as two legs on the silk. However, P. phalangioides does not attack prey that is completely away from webs. Occasionally, P. phalangioides feeds on eggs of other spiders and on ensnared insects it encounters in alien webs. Experimental evidence indicates that vision is of little or no importance in the predatory behaviour of P. phalangioides . Although P. phalangioides invades diverse types of webs, in addition to using its own web, its efficiency as a predator varies with web-type. It is most efficient as a predator of spiders and, especially, insects on its own web, and least efficient as a predator of amaurobiids on their cribellate sheet webs. Sensory, locomotory and other factors which influence differential predatory efficiency are discussed. The behaviour of P. phalangioides is compared to that of Portia , an araneophagic web-invading salticid, and the results of this study are discussed in relation to hypotheses concerning salticid evolution.     

The phylogenetic placement of Psechridae within Entelegynae and the convergent origin of orb‐like spider webs

Evolutionary convergence of phenotypic traits provides evidence for their functional success. The origin of the orb web was a critical event in the diversification of spiders that facilitated a spectacular radiation of approximately 12 000 species and promoted the evolution of novel web types. How the orb web evolved from ancestral web types, and how many times orb‐like architectures evolved in spiders, has been debated for a long time. The little known spider genus Fecenia (Psechridae) constructs a web that resembles the archetypical orb web, but morphological data suggest that Psechridae (Psechrus + Fecenia) does not belong in Orbiculariae, the ‘true orb weavers’, but to the ‘retrolateral tibial apophysis (RTA) clade’ consisting mostly of wandering spiders, but also including spiders building less regular webs. Yet, the data are sparse and no molecular phylogenetic study has estimated Fecenia's exact position in the tree of life. Adding new data to sequences pulled from GenBank, we reconstruct a phylogeny of Entelegynae and phylogenetically test the monophyly and placement of Psechridae, and in doing so, the alternative hypotheses of monophyletic origin of the orb web and the pseudo‐orb versus their independent origins, a potentially spectacular case of behavioural convergence. We also discuss the implications of our results for Entelegynae systematics. Our results firmly place a monophyletic Psechridae within the RTA clade, phylogenetically distant from true orb weavers. The architectural similarities of the orb and the pseudo‐orb are therefore clearly convergent, as also suggested by detailed comparisons of these two web types, as well as the spiders' web‐building behaviours and ontogenetic development. The convergence of Fecenia webs with true orbs provides a remarkable opportunity to investigate how these complex sets of traits may have interacted during the evolution of the orb.     

Resting metabolic rates of two orbweb spiders: a first approach to evolutionary success of ecribellate spiders

Spiders are considered conservative with regard to their resting metabolic rate, presenting the same allometric relation with body mass as the majority of land-arthropods. Nevertheless, web-building is thought to have a great impact on the energetic metabolism, and any modification that affects this complex behavior is expected to have an impact over the daily energetic budget. We analyzed the possibility of the presence of the cribellum having an effect on the allometric relation between resting metabolic rate and body mass for an ecribellate species (Zosis geniculata) and a cribellate one (Metazygia rogenhoferi), and employed a model selection approach to test if these species had the same allometric relationship as other land-arthropods. Our results show that M. rogenhoferi has a higher resting metabolic rate, while Z. geniculata fitted the allometric prediction for land arthropods. This indicates that the absence of the cribellum is associated with a higher resting metabolic rate, thus explaining the higher promptness to activity found for the ecribellate species. If our result proves to be a general rule among spiders, the radiation of Araneoidea could be connected to a more energy-consuming life style. Thus, we briefly outline an alternative model of diversification of Araneoidea that accounts for this possibility.     

Evolution of aerial spider webs coincided with repeated structural optimization of silk anchorages

Physical structures built by animals challenge our understanding of biological processes and inspire the development of smart materials and green architecture. It is thus indispensable to understand the drivers, constraints, and dynamics that lead to the emergence and modification of building behavior. Here, we demonstrate that spider web diversification repeatedly followed strikingly similar evolutionary trajectories, guided by physical constraints. We found that the evolution of suspended webs that intercept flying prey coincided with small changes in silk anchoring behavior with considerable effects on the robustness of web attachment. The use of nanofiber based capture threads (cribellate silk) conflicts with the behavioral enhancement of web attachment, and the repeated loss of this trait was frequently followed by physical improvements of web anchor structure. These findings suggest that the evolution of building behavior may be constrained by major physical traits limiting its role in rapid adaptation to a changing environment.     

The Trochidae and Turbinidae of the Kermadec Ridge (Mollusca: Gastropoda)

Abstract

Taieria erebus (Gnaphosidae) was found to be a versatile predator: it captured insects both cursorially (away from webs) and kleptopar-asitically (on alien webs); it captured spiders in both the presence and absence of webs; and it also ate the eggs of host spiders (oophagy). When T. erebus invaded webs, it was as an aggressive mimic — it performed a repertoire of vibratory behaviours to lure the host spider. Although T. erebus pursued and captured spiders on diverse web-types, it was more effective as a predator when invading densely (rather than sparsely) woven cribellate and non-sticky webs, and was especially effective on non-cribellate sticky webs. Gnaphosids are traditionally referred to as hunting spiders, but T. erebus built a small prey-capture web. T. erebus also preyed on segestriid spiders, then used their webs to catch more prey, this being an unusual example of a spider using, as a tool for predation, the spinning-work of another species from an unrelated family. T. erebus used specialised behaviours to prey on nesting cursorial spiders. Prey was either grasped or stabbed; the venom of T. erebus was highly potent against spiders. Experiments indicated that vision was of little or no importance in the predatory behaviour of T. erebus. The behaviour of T. erebus is compared to that of Portia, a web-building salticid spider which is very versatile in its predatory behaviour and has acute vision. T. erebus is discussed in relation to hypotheses concerning gnaphosid and salticid evolution.     

The long and short of sperm polymorphisms in insects

Production of more than one morphological type of sperm in a common testis has been documented for a variety of invertebrates, including gastropods, spiders, centipedes, and insects. This unusual phenomenon is difficult to explain by current theory, particularly since available evidence indicates that one sperm type is often incapable of effecting fertilization. In this review we critically examine evidence on the distribution and development of sperm heteromorphisms among insects in light of competing hypotheses for the evolutionary origin, maintenance, and function of a non-fertilizing class of sperm. To date, no single hypothesis, including alternatives which assume non-fertilizing sperm are non-adaptive, or that they provision, facilitate, or compete with fertilizing sperm, has received strong empirical support by any group of insects. The diversity of sperm heteromorphisms suggests that non-fertilizing sperm may have different functions in different clades or even serve multiple functions within a clade. We suggest that insight could be gained from (1) new models for the evolution of sperm polymorphism, (2) comparative studies that focus on multiple traits simultaneously (e.g. sperm number, proportion, length, and remating rate) and utilize clades in which more than one gain or loss of sperm heteromorphism has been documented (e.g. Pentatomidae, Carabidae, or Diopsidae), and (3) experimental studies that exploit individual variation or directly manipulate the composition of the male ejaculate.     

Correlates of rate heterogeneity in avian ecomorphological traits

Heterogeneity in rates of trait evolution is widespread, but it remains unclear which processes drive fast and slow character divergence across global radiations. Here, we test multiple hypotheses for explaining rate variation in an ecomorphological trait (beak shape) across a globally distributed group (birds). We find low support that variation in evolutionary rates of species is correlated with life history, environmental mutagenic factors, range size, number of competitors, or living on islands. Indeed, after controlling for the negative effect of species' age, 80% of variation in species‐specific evolutionary rates remains unexplained. At the clade level, high evolutionary rates are associated with unusual phenotypes or high species richness. Taken together, these results imply that macroevolutionary rates of ecomorphological traits are governed by both ecological opportunity in distinct adaptive zones and niche differentiation among closely related species.     

Trophic specialisation in a predatory group: the case of prey‐specialised spiders (Araneae)

Predators appear to be less frequently specialised (i.e. adapted to restricted diet) on their prey than herbivores, parasites or parasitoids. Here, we critically evaluate contemporary evolutionary hypotheses that might be used to explain the evolution of specialised foraging in predators. We propose a unifying concept within which we define four types of trophic categories using ecological (diet breadth) and evolutionary (degree of adaptations) contexts. We use data on spiders (Araneae), the most diversified order of terrestrial predators, to assess applicability of frameworks and evolutionary concepts related to trophic specialisation. The majority of spider species are euryphagous but a few have a restricted prey range, i.e. they are stenophagous. We provide a detailed overview of specialisation on different prey types, namely spiders, crustaceans, moths, dipterans, ants, and termites. We also review the available evidence for trophic adaptations, classified into four categories: behavioural, morphological, venomic and metabolic. Finally, we discuss the ecological and evolutionary implications of trophic specialisation and propose avenues for future research.     

Kleptoparasites influence foraging behaviour of the spider <Emphasis Type="Italic">Stegodyphus lineatus</Emphasis> (Araneae,Eresidae)

Prey captured by a predator may attract kleptoparasites which could significantly reduce the amount of food consumed. Stegodyphus lineatus, a cribellate spider, builds an energetically costly web. Ants raid the webs of S. lineatus to steal prey and behave as kleptoparasites. We investigated ant raids in a natural population of S. lineatus and their influence on the spider’s foraging behaviour. Considering spiders that had captured a prey, 31.2% suffered an ant raid within 24 h after the prey capture. Experimental tests showed that the response to ant raid is to delay web rebuilding and this was independent of a spider’s previous foraging success. There was a tendency for spiders that were exposed to ants to build larger webs. Neither prey-handling duration nor prey consumption was modified after exposure to ants. These results suggest that Stegodyphus lineatus adapt its web-building behaviour in response to the risk of kleptoparasitism.