Vestigial organs alter fossil placements in an ancient group of terrestrial chelicerates.

Vestigial organs provide a link between ancient and modern traits and therefore have great potential to resolve the phylogeny of contentious fossils that bear features not seen in extant species. Here we show that extant daddy-longlegs (Arachnida, Opiliones), a group once thought to possess only one pair of eyes, in fact additionally retain a pair of vestigial median eyes and a pair of vestigial lateral eyes. Neuroanatomical gene expression surveys of eye-patterning transcription factors, opsins, and other structural proteins in the daddy-longlegs Phalangium opilio show that the vestigial median and lateral eyes innervate regions of the brain positionally homologous to the median and lateral eye neuropils, respectively, of chelicerate groups like spiders and horseshoe crabs. Gene silencing of eyes absent shows that the vestigial eyes are under the control of the retinal determination gene network. Gene silencing of dachshund disrupts the lateral eyes, but not the median eyes, paralleling loss-of-function phenotypes in insect models. The existence of lateral eyes in extant daddy-longlegs bears upon the placement of the oldest harvestmen fossils, a putative stem group that possessed both a pair of median eyes and a pair of lateral eyes. Phylogenetic analysis of harvestman relationships with an updated understanding of lateral eye incidence resolved the four-eyed fossil group as a member of the extant daddy-longlegs suborder, which in turn resulted in older estimated ages of harvestman diversification. This work underscores that developmental vestiges in extant taxa can influence our understanding of character evolution, placement of fossils, and inference of divergence times.

Phylogenomic data reveal three new families of poorly studied Solifugae (camel spiders).

The systematics of the arachnid order Solifugae have been an enigma, owing to challenges in interpreting morphology, a paucity of molecular phylogenetic studies sampling across the group, and a dearth of taxonomic attention for many lineages. Recent work has suggested that solifuge families largely exhibit contiguous distributions and reflect patterns of vicariance, with the exception of three families: Melanoblossidae, Daesiidae and Gylippidae. Morphological studies have cast doubt on their existing circumscriptions and the present composition of these taxa renders their distributions as disjunct. We leveraged ultraconserved elements (UCEs) to test the phylogenetic placement of three key lineages of Solifugae that cause these anomalous distributions: Dinorhax rostrumpsittaci (putative melanoblossid), Namibesia (putative daesiid), and Trichotoma (putative gylippid). Phylogenetic placement of these three genera based on UCEs rendered the families that harbor them as para- or polyphyletic, recovering instead relationships that better accord with a biogeographic history driven by vicariance. Toward a stable and phylogenetically informed classification of Solifugae, we establish three new families, Dinorhaxidae new rank, Namibesiidae new rank and Lipophagidae new rank.

Effects of Natural Habitat and Season on Cursorial Spider Assemblages in Mediterranean Vineyards.

Natural habitats adjacent to vineyards are presumed to have a positive effect on the diversity of natural enemies within the vineyards. However, these habitats differ in vegetation structure and seasonal phenology and in turn could affect the species composition of natural enemies. Here, we compared the species richness and diversity and the composition of spider assemblages in several locations within three commercial vineyards and the nearby natural habitats in a Mediterranean landscape in northern Israel. We sampled spiders by means of pitfall traps in early and in late summer. Both the time in the season and the habitat (natural versus vineyard) affected spider species richness and diversity. More species were found in early summer (47) than in late summer (33), and more occurred in the natural habitat (34 species) than in the vineyards (27-31 species). Fifteen species were found exclusively in the natural habitat, and only 11 species were shared by the vineyards and natural habitat, four of which were the most abundant and geographically widely distributed species in the samples. In late summer, spider diversity in the natural habitat was higher than within the vineyards: the spider assemblages in the vineyards became dominated by a few species late in the crop season, while those of the natural habitat remained stable. Overall, the natural habitat differed in assemblage composition from all within-vineyard locations, while the three locations within the vineyard did not differ significantly in assemblage composition. Season (early vs. late summer), however, significantly affected the spider assemblage composition. This study documents the large diversity of spiders in a local Mediterranean vineyard agroecosystem. Over 60% of the known spider families in the region occurred in our samples, highlighting the importance of this agroecosystem for spider diversity and the potential for conservation biocontrol, where natural habitats may be a source of natural enemies for nearby vineyards.

Neglected no longer: Phylogenomic resolution of higher-level relationships in Solifugae.

Advanced sequencing technologies have expedited resolution of higher-level arthropod relationships. Yet, dark branches persist, principally among groups occurring in cryptic habitats. Among chelicerates, Solifugae ("camel spiders") is the last order lacking a higher-level phylogeny and have thus been historically characterized as "neglected [arachnid] cousins". Though renowned for aggression, remarkable running speed, and xeric adaptation, inferring solifuge relationships has been hindered by inaccessibility of diagnostic morphological characters, whereas molecular investigations have been limited to one of 12 recognized families. Our phylogenomic dataset via capture of ultraconserved elements sampling all extant families recovered a well-resolved phylogeny, with two distinct groups of New World taxa nested within a broader Paleotropical radiation. Divergence times using fossil calibrations inferred that Solifugae radiated by the Permian, and most families diverged prior to the Paleogene-Cretaceous extinction, likely driven by continental breakup. We establish Boreosolifugae new suborder uniting five Laurasian families, and Australosolifugae new suborder uniting seven Gondwanan families using morphological and biogeographic signal.

In the land of the blind: Exceptional subterranean speciation of cryptic troglobitic spiders of the genus Tegenaria (Araneae: Agelenidae) in Israel.

Caves have long been recognized as a window into the mechanisms of diversification and convergent evolution, due to the unique conditions of isolation and life in the dark. These lead to adaptations and reduce dispersal and gene flow, resulting in high levels of speciation and endemism. The Israeli cave arachnofauna remains poorly known, but likely represents a rich assemblage. In a recent survey, we found troglophilic funnel-web spiders of the genus Tegenaria in 26 caves, present mostly at the cave entrance ecological zone. In addition, we identified at least 14 caves inhabited by troglobitic Tegenaria, which are present mostly in the twilight and dark ecological zones. Ten of the caves, located in the north and center of Israel, are inhabited by both troglophilic and troglobitic Tegenaria. These spiders bear superficial phenotypic similarities but differ in the levels of eye reduction and pigmentation. To test whether these taxa constitute separate species, as well as understand their relationships to epigean counterparts, we conducted a broad geographic sampling of cave-dwelling Tegenaria in Israel and Palestine, using morphological and molecular evidence. Counterintuitively, our results show that the troglobitic Tegenaria we studied are distantly related to the troglophilic Tegenaria found at each of the cave entrances we sampled. Moreover, seven new troglobitic species can be identified based on genetic differences, eye reduction level, and features of the female and male genitalia. Our COI analysis suggest that the Israeli troglobitic Tegenaria species are more closely related to eastern-Mediterranean congeners than to the local sympatric troglophile Tegenaria species, suggesting a complex biogeographic history.

The global spread of misinformation on spiders.

In the internet era, the digital architecture that keeps us connected and informed may also amplify the spread of misinformation. This problem is gaining global attention, as evidence accumulates that misinformation may interfere with democratic processes and undermine collective responses to environmental and health crises1,2. In an increasingly polluted information ecosystem, understanding the factors underlying the generation and spread of misinformation is becoming a pressing scientific and societal challenge3. Here, we studied the global spread of (mis-)information on spiders using a high-resolution global database of online newspaper articles on spider-human interactions, covering stories of spider-human encounters and biting events published from 2010-20204. We found that 47% of articles contained errors and 43% were sensationalist. Moreover, we show that the flow of spider-related news occurs within a highly interconnected global network and provide evidence that sensationalism is a key factor underlying the spread of misinformation.

Recent speciation and phenotypic plasticity within a parthenogenetic lineage of levantine whip spiders (Chelicerata: Amblypygi: Charinidae).

Caves constitute ideal study systems for investigating adaptation and speciation, as the abiotic conditions shared by aphotic habitats exert a set of environmental filters on their communities. Arachnids constitute an important component of many cave ecosystems worldwide. We investigated the population genomics of two whip spider species: Sarax ioanniticus, a widely distributed parthenogenetic species found across the eastern Mediterranean; and S. israelensis, a recently described troglomorphic species that is endemic to caves in Israel. Here, we show that S. israelensis is completely genetically distinct from S. ioanniticus and most likely also a parthenogen. Counterintuitively, despite the lack of genetic variability within S. ioanniticus and S. israelensis, we discovered considerable variation in the degree of median eye reduction, particularly in the latter species. Natural history data from captive-bred specimens of S. israelensis validated the interpretation of parthenogenesis. Our results are most consistent with a scenario of a sexual ancestral species that underwent speciation, followed by independent transitions to apomictic parthenogenesis in each of the two daughter species. Moreover, the lack of genetic variability suggests that variation in eye morphology in S. israelensis is driven exclusively by epigenetic mechanisms.

Phylogenomics of Scorpions Reveal Contemporaneous Diversification of Scorpion Mammalian Predators and Mammal-Active Sodium Channel Toxins.

Scorpions constitute a charismatic lineage of arthropods and comprise more than 2500 described species. Found throughout various tropical and temperate habitats, these predatory arachnids have a long evolutionary history, with a fossil record that began in the Silurian. While all scorpions are venomous, the asymmetrically diverse family Buthidae harbors nearly half the diversity of extant scorpions, and all but one of the 58 species that are medically significant to humans. However, the lack of a densely sampled scorpion phylogeny has hindered broader inferences of the diversification dynamics of scorpion toxins. To redress this gap, we assembled a phylogenomic data set of 100 scorpion venom gland transcriptomes and genomes, emphasizing the sampling of highly toxic buthid genera. To infer divergence times of venom gene families, we applied a phylogenomic node dating approach for the species tree in tandem with phylostratigraphic bracketing to estimate the minimum ages of mammal-specific toxins. Our analyses establish a robustly supported phylogeny of scorpions, particularly with regard to relationships between medically significant taxa. Analysis of venom gene families shows that mammal-active sodium channel toxins (NaTx) have independently evolved in five lineages within Buthidae. Temporal windows of mammal-targeting toxin origins are correlated with the basal diversification of major scorpion mammal predators such as shrews, bats, and rodents. These results suggest an evolutionary model of relatively recent diversification of buthid NaTx homologs in response to the diversification of scorpion predators. [Adaptation; arachnids; phylogenomic dating; phylostratigraphy; venom.].

An expert-curated global database of online newspaper articles on spiders and spider bites.

Mass media plays an important role in the construction and circulation of risk perception associated with animals. Widely feared groups such as spiders frequently end up in the spotlight of traditional and social media. We compiled an expert-curated global database on the online newspaper coverage of human-spider encounters over the past ten years (2010-2020). This database includes information about the location of each human-spider encounter reported in the news article and a quantitative characterisation of the content-location, presence of photographs of spiders and bites, number and type of errors, consultation of experts, and a subjective assessment of sensationalism. In total, we collected 5348 unique news articles from 81 countries in 40 languages. The database refers to 211 identified and unidentified spider species and 2644 unique human-spider encounters (1121 bites and 147 as deadly bites). To facilitate data reuse, we explain the main caveats that need to be made when analysing this database and discuss research ideas and questions that can be explored with it.

Comprehensive Species Sampling and Sophisticated Algorithmic Approaches Refute the Monophyly of Arachnida.

Deciphering the evolutionary relationships of Chelicerata (arachnids, horseshoe crabs, and allied taxa) has proven notoriously difficult, due to their ancient rapid radiation and the incidence of elevated evolutionary rates in several lineages. Although conflicting hypotheses prevail in morphological and molecular data sets alike, the monophyly of Arachnida is nearly universally accepted, despite historical lack of support in molecular data sets. Some phylotranscriptomic analyses have recovered arachnid monophyly, but these did not sample all living orders, whereas analyses including all orders have failed to recover Arachnida. To understand this conflict, we assembled a data set of 506 high-quality genomes and transcriptomes, sampling all living orders of Chelicerata with high occupancy and rigorous approaches to orthology inference. Our analyses consistently recovered the nested placement of horseshoe crabs within a paraphyletic Arachnida. This result was insensitive to variation in evolutionary rates of genes, complexity of the substitution models, and alternative algorithmic approaches to species tree inference. Investigation of sources of systematic bias showed that genes and sites that recover arachnid monophyly are enriched in noise and exhibit low information content. To test the impact of morphological data, we generated a 514-taxon morphological data matrix of extant and fossil Chelicerata, analyzed in tandem with the molecular matrix. Combined analyses recovered the clade Merostomata (the marine orders Xiphosura, Eurypterida, and Chasmataspidida), but merostomates appeared nested within Arachnida. Our results suggest that morphological convergence resulting from adaptations to life in terrestrial habitats has driven the historical perception of arachnid monophyly, paralleling the history of numerous other invertebrate terrestrial groups.

Five-Year Monitoring of a Desert Burrow-Dwelling Spider Following an Environmental Disaster Indicates Long-Term Impacts.

Deserts are characterized by unpredictable precipitation and extreme temperatures. Their fauna and flora are sensitive to anthropogenic environmental changes, and often recover slowly from environmental disasters. The effects of oil spills on the biota of desert regions, however, have scarcely been studied. We predicted that terrestrial invertebrates suffer long-term negative effects from an oil spill, due to their close association with the substrate. Thus, we investigated the effects of two oil spills that occurred in 1975 and 2014 in the hyper-arid 'Arava desert (Israel), on a spider that constructs silk-lined nests in burrows in compact, sandy soil in this extreme desert habitat. The spider, Sahastata aravaensis sp. nov. (Filistatidae), is described herein. We assessed spider burrow abundance in plots located in oil-contaminated and nearby uncontaminated clean soil (control) areas over five consecutive years and measured habitat characteristics in these plots. In the laboratory, we determined the preference of individuals for clean vs. oil-contaminated soil as a resting substrate. Finally, as this species was previously undescribed, we added a new species description. The abundance of Sahastata was significantly lower in oil-contaminated plots, and this was the case in the 40-year-old oil spill (1975) as well as in the recent one (2014). In laboratory tests, spiders showed a significant preference for the clean soil substrate over the oil-contaminated substrate. In the field, soil crust hardness and vegetation density did not differ significantly between oil-contaminated and control plots, but these measures were highly variable. The burrows were significantly clustered, suggesting that the young disperse only short distances. In the laboratory adult spiders did not dig burrows, perhaps indicating that adults remain permanently in their natal burrows and that in the field they may use vacant burrows. We conclude that Sahastata populations were affected negatively by the oil spills and these effects were long-lasting. We propose that by monitoring their spatial distribution, burrow-dwelling spiders such as Sahastata can be used as effective bioindicators of soil pollution in desert habitats.

Taxonomic Sampling and Rare Genomic Changes Overcome Long-Branch Attraction in the Phylogenetic Placement of Pseudoscorpions.

Long-branch attraction is a systematic artifact that results in erroneous groupings of fast-evolving taxa. The combination of short, deep internodes in tandem with long-branch attraction artifacts has produced empirically intractable parts of the Tree of Life. One such group is the arthropod subphylum Chelicerata, whose backbone phylogeny has remained unstable despite improvements in phylogenetic methods and genome-scale data sets. Pseudoscorpion placement is particularly variable across data sets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount long-branch attraction, we investigated the effect of taxonomic sampling via sequential deletion of basally branching pseudoscorpion superfamilies, as well as varying gene occupancy thresholds in supermatrices. We show that concatenated supermatrices and coalescent-based summary species tree approaches support a sister group relationship of pseudoscorpions and scorpions, when more of the basally branching taxa are sampled. Matrix completeness had demonstrably less influence on tree topology. As an external arbiter of phylogenetic placement, we leveraged the recent discovery of an ancient genome duplication in the common ancestor of Arachnopulmonata as a litmus test for competing hypotheses of pseudoscorpion relationships. We generated a high-quality developmental transcriptome and the first genome for pseudoscorpions to assess the incidence of arachnopulmonate-specific duplications (e.g., homeobox genes and miRNAs). Our results support the inclusion of pseudoscorpions in Arachnopulmonata (new definition), as the sister group of scorpions. Panscorpiones (new name) is proposed for the clade uniting Scorpiones and Pseudoscorpiones.

Systemic paralogy and function of retinal determination network homologs in arachnids.

BACKGROUND: Arachnids are important components of cave ecosystems and display many examples of troglomorphisms, such as blindness, depigmentation, and elongate appendages. Little is known about how the eyes of arachnids are specified genetically, let alone the mechanisms for eye reduction and loss in troglomorphic arachnids. Additionally, duplication of Retinal Determination Gene Network (RDGN) homologs in spiders has convoluted functional inferences extrapolated from single-copy homologs in pancrustacean models. RESULTS: We investigated a sister species pair of Israeli cave whip spiders, Charinus ioanniticus and C. israelensis (Arachnopulmonata, Amblypygi), of which one species has reduced eyes. We generated embryonic transcriptomes for both Amblypygi species, and discovered that several RDGN homologs exhibit duplications. We show that duplication of RDGN homologs is systemic across arachnopulmonates (arachnid orders that bear book lungs), rather than being a spider-specific phenomenon. A differential gene expression (DGE) analysis comparing the expression of RDGN genes in field-collected embryos of both species identified candidate RDGN genes involved in the formation and reduction of eyes in whip spiders. To ground bioinformatic inference of expression patterns with functional experiments, we interrogated the function of three candidate RDGN genes identified from DGE using RNAi in the spider Parasteatoda tepidariorum. We provide functional evidence that one of these paralogs, sine oculis/Six1 A (soA), is necessary for the development of all arachnid eye types. CONCLUSIONS: Our work establishes a foundation to investigate the genetics of troglomorphic adaptations in cave arachnids, and links differential gene expression to an arthropod eye phenotype for the first time outside of Pancrustacea. Our results support the conservation of at least one RDGN component across Arthropoda and provide a framework for identifying the role of gene duplications in generating arachnid eye diversity.

Trunk Refugia: A Simple, Inexpensive Method for Sampling Tree Trunk Arthropods.

Trees host a large share of the global arthropod diversity. Several methodologies have been described to sample arthropods from trees, ranging from active sampling techniques (e.g., visual searching, beating, or shaking the branches) to passive sampling devices. The majority of these collection techniques are destructive, and do not specifically target the tree trunk arthropod fauna. Here, we describe an alternative sampling method called trunk refugia (TR). TR are cylindrical shelters made of corrugated cardboard that can be secured to trees using string, and can remain exposed for varying time periods. These refugia are inexpensive, easy to use, and suitable to monitor a diverse array of insects and arachnids. Moreover, TR are nonlethal sampling tools, and allow collecting live individuals for behavioral studies or for rearing.

Ordered phylogenomic subsampling enables diagnosis of systematic errors in the placement of the enigmatic arachnid order Palpigradi.

The miniaturized arachnid order Palpigradi has ambiguous phylogenetic affinities owing to its odd combination of plesiomorphic and derived morphological traits. This lineage has never been sampled in phylogenomic datasets because of the small body size and fragility of most species, a sampling gap of immediate concern to recent disputes over arachnid monophyly. To redress this gap, we sampled a population of the cave-inhabiting species Eukoenenia spelaea from Slovakia and inferred its placement in the phylogeny of Chelicerata using dense phylogenomic matrices of up to 1450 loci, drawn from high-quality transcriptomic libraries and complete genomes. The complete matrix included exemplars of all extant orders of Chelicerata. Analyses of the complete matrix recovered palpigrades as the sister group of the long-branch order Parasitiformes (ticks) with high support. However, sequential deletion of long-branch taxa revealed that the position of palpigrades is prone to topological instability. Phylogenomic subsampling approaches that maximized taxon or dataset completeness recovered palpigrades as the sister group of camel spiders (Solifugae), with modest support. While this relationship is congruent with the location and architecture of the coxal glands, a long-forgotten character system that opens in the pedipalpal segments only in palpigrades and solifuges, we show that nodal support values in concatenated supermatrices can mask high levels of underlying topological conflict in the placement of the enigmatic Palpigradi.

Linking morphological and molecular taxonomy for the identification of poultry house, soil, and nest dwelling mites in the Western Palearctic.

Because of its ability to expedite specimen identification and species delineation, the barcode index number (BIN) system presents a powerful tool to characterize hyperdiverse invertebrate groups such as the Acari (mites). However, the congruence between BINs and morphologically recognized species has seen limited testing in this taxon. We therefore apply this method towards the development of a barcode reference library for soil, poultry litter, and nest dwelling mites in the Western Palearctic. Through analysis of over 600 specimens, we provide DNA barcode coverage for 35 described species and 70 molecular taxonomic units (BINs). Nearly 80% of the species were accurately identified through this method, but just 60% perfectly matched (1:1) with BINs. High intraspecific divergences were found in 34% of the species examined and likely reflect cryptic diversity, highlighting the need for revision in these taxa. These findings provide a valuable resource for integrative pest management, but also highlight the importance of integrating morphological and molecular methods for fine-scale taxonomic resolution in poorly-known invertebrate lineages.

Does mating disruption of Planococcus ficus and Lobesia botrana affect the diversity, abundance and composition of natural enemies in Israeli vineyards?

BACKGROUND: Mating disruption (MD) employs high doses of a pest's synthetic sex pheromone in agricultural plots, to interfere with its reproduction. MD is assumed to have few behavioral effects on non-target arthropods, because sex pheromones are highly species-specific and non-toxic. Nevertheless, some natural enemies use their host's sex pheromones as foraging cues, and thus may be attracted to MD plots. To investigate this hypothesis, we compared parasitoid and spider assemblages in paired plots in five Israeli vineyards during 2015. One plot was MD-treated against two key pests, Lobesia botrana (Denis & Schiffermüller) and Planococcus ficus (Signoret). Both plots were insecticide-treated as needed. Natural enemies were suction-sampled and collected from pheromone-baited monitoring traps. RESULTS: The total abundance, species diversity and species composition of most natural enemies were unaffected by MD. An important exception involved P. ficus' main parasitoid, Anagyrus sp. nr. pseudococci (Girault). Anagyrus sp. nr. pseudococci females were mainly captured in control plots, while male captures were low and not influenced by MD. Parasitized P. ficus occurred only in MD plots. CONCLUSION: Non-target effects of MD involved mostly A. sp. nr. pseudococci females and hardly affected other natural enemies. These findings support the use of MD as an environmentally friendly pest management strategy. © 2018 Society of Chemical Industry.