Biological photonic systems composed of anhydrous guanine crystals evolved separately in several taxonomic groups. Here, two such systems found in fish and spiders, both of which make use of anhydrous guanine crystal plates to produce structural colors, are examined. Measurements of the photonic‐crystal structures using cryo‐SEM show that the crystal plates in both fish skin and spider integument are ∼20‐nm thick. The reflective unit in the fish comprises stacks of single plates alternating with ∼230‐nm‐thick cytoplasm layers. In the spiders the plates are formed as doublet crystals, cemented by 30‐nm layers of amorphous guanine, and are stacked with ∼200 nm of cytoplasm between crystal doublets. They achieve light reflective properties through the control of crystal morphology and stack dimensions, reaching similar efficiencies of light reflectivity in both fish skin and spider integument. The structure of guanine plates in spiders are compared with the more common situation in which guanine occurs in the form of relatively unorganized prismatic crystals, yielding a matt white coloration.
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 LBA 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 datasets. Pseudoscorpion placement is particularly variable across datasets and analytical frameworks, with this group either clustering with other long-branch orders or with Arachnopulmonata (scorpions and tetrapulmonates). To surmount LBA, 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.
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.
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. While conflicting hypotheses prevail in morphological and molecular datasets alike, the monophyly of Arachnida is nearly universally accepted, despite historical lack of support in molecular datasets. 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 dataset 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.
Generalist predators contribute to pest suppression in agroecosystems. Spider communities, which form a substantial fraction of the generalist predator fauna in arable land, are characterized by two functional groups: web-building and cursorial (non-web-building) species. We investigated the relative impact of these two functional groups on a common pest (Sitobion avenae, Aphididae) in wheat by combining a molecular technique that revealed species-specific aphid consumption rates with a factorial field experiment that analyzed the impact, separately and together, of equal densities of these two spider functional groups on aphid population growth. Only cursorial spiders retarded aphid population growth in our cage experiment, but this effect was limited to the initial aphid-population growth period and low-to-intermediate aphid densities. The molecular analysis, which used aphid-specific primers to detect aphid DNA in predator species, detected the highest proportion of aphid-consuming individuals in two cursorial spiders: the foliage-dwelling Xysticus cristatus (Thomisidae) and the ground-active Pardosa palustris (Lycosidae). The results suggest that manipulating the community composition in favour of pest-consuming functional groups may be more important for improving biological control than fostering predator biodiversity per se. Agricultural management practices that specifically foster effective species or functional groups (e.g. mulching for cursorial spiders) should receive more attention in low-pesticide farming systems.
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.]
1. Arthropods living in annual crops suffer mortality caused by agricultural practices. Therefore, migration from surrounding habitats is crucial to maintain populations of natural enemies of insect pests in crops. In desert agroecosystems there is a pronounced contrast between managed and unmanaged habitats, where irrigated and fertilised crops are islands of productivity in an arid matrix. This contrast could either enhance or inhibit movement of natural enemies between the landscape components.2. The importance of the surrounding arid habitats as a source for spiders in crops was examined in the Negev desert of Israel. Spiders were sampled in both arid natural habitat and adjacent wheat fields using pitfall traps and visual searching. In addition, spiders in wheat fields were sampled throughout the winter cropping season using emergence traps at increasing distances from the field edge. Stationary and movable emergence traps were used to distinguish between residents and migrant species.3. The spider assemblage in the wheat was dominated by three families: Linyphiidae, Theridiidae, and Gnaphosidae. Spider sampling in both natural arid habitat and adjacent wheat fields enabled four functional groups to be recognised that differed in habitat preference, movement patterns, and population dynamics. Thirty‐three per cent of collected individuals were classified as crop residents whereas more than 50% were classified as migrants from the surrounding habitats. These findings suggest that the surrounding habitats influence spider assemblage composition in the fields, in spite of the marked contrast in habitat structure and productivity.4. Spider assemblages in the wheat fields were dominated by migrant species arriving from the surrounding arid habitats. Migrant spiders inhabited the crop throughout the cropping season. The combined contribution of resident and migrant functional groups may act to prevent insect pest outbreaks in this desert agroecosystem.
Intensively cultivated arable land and semi-desert are two dominant habitat types in the arid agroecosystem in the northwest Negev Desert (Israel). The present study compares activity-densities and species richness of spiders in these distinctive habitat types. Sixteen wheat fields and twelve locations in the semi-desert were sampled during the winter growing season of wheat. Semi-desert habitats had more spider species and higher spider activity-densities than irrigated wheat fields. The majority of spider families, namely Gnaphosidae, Thomisidae, Salticidae, Zodariidae, Philodromidae, Dysderidae, and Clubionidae had significantly higher activity-densities in the semi-desert compared to wheat. Only two families, the Linyphiidae that strongly dominated the arable spider community and Corinnidae had higher activitydensities in wheat than in semi-desert. Out of a total of 94 spider species, fourteen had significantly higher activity-densities in semi-desert than in wheat fields and eight species had significantly higher activity-densities in wheat fields than in semidesert. Spider families and species that dominated the semi-desert communities also occurred in the wheat fields but at lower activity-densities. In conclusion, the semi-desert is a potential source of spider species and families that may immigrate into arable fields during winter. In particular, active hunting spiders may be sustained in crops through immigration from nearby semi-desert habitats.
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