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.].

A unique yet technically simple type of joint allows for the high mobility of scorpion tails.

Although being one of the most well-known animal groups, functional and constructional aspects of scorpions and especially of their tail (metasoma) have so far been overlooked. This tail represents a special construction, as it consists of five tube-shaped segments made up of strong cuticle, which are movable against each other and thus manoeuvre the notorious stinger both quickly and very precisely in space. This high mobility of an exoskeletal structure can be attributed to the connection between the segments described here for the first time. This joint allows for the twisting and bending at the same time in a single, simple construction: adjoining metasomal segments each possess an almost circular opening posteriorly, where the next segment is lodged. Anteriorly, these segments possess two saddle-like protrusions laterally, which are able to rotate in two directions on the rim of the posterior circular opening of the previous segment allowing for twisting and bending. The metasomal joint is particularly noteworthy since its mechanism can be compared to that of arthropod appendages. The scorpion metasoma is actually the only known case in Chelicerata, in which an entire body section has been modified to perform tasks similar to that of an appendage while containing digestive organs. The joint mechanism can also inspire technical applications, for instance in robotics.

Comparative morphology of scorpion metasomata: Muscles and cuticle.

Scorpions are among the most popular research objects within Arachnida and there is an impressive body of knowledge about their biology, distribution, morphology, etc. Although the poison sting has gained a lot of attention due to its potential lethal effects to humans, hitherto, there has been no comparative morphological study on the metasoma, the body part that delivers the poisonous injection. The metasoma always consists of five body segments terminated by a poison sting, but it presents significant morphological variations, both between sexes and between species. Its form ranges from long and thin to short and rather reduced to thick and dominant. In this study, we investigated species representing major scorpion clades and most of the known morphological disparity. Using high-resolution micro-computer-tomography and 3D-reconstruction, we present the first 3D visualizations of metasomal exo-skeletal elements in combination with their musculature. Despite of morphological varying metasomal forms, in all investigated species, a repeating pattern of muscles was found: four pairs of muscles in metasomal segment one to four and two pairs of muscles in metasomal segment five. However, the metasomal muscles are characterized by an antero-posterior change in their shapes and sizes and interspecific variation was also found in the extrinsic metasomal musculature, i.e. the muscles that link metasoma to mesosoma.

Phylogenomics facilitates stable scorpion systematics: Reassessing the relationships of Vaejovidae and a new higher-level classification of Scorpiones (Arachnida).

The Neartic family Vaejovidae (Scorpiones: Chactoidea) has long been treated as a diverse and systematically cohesive group of scorpions, but its monophyly and relationship to other scorpion families have historically been questioned. Morphological data have supported its monophyly and a variety of phylogenetic placements within the superfamily Chactoidea. Recent phylogenomic analyses have instead recovered vaejovids as polyphyletic (albeit with minimal taxonomic sampling) and Chactoidea as paraphyletic. Here, we reexamined the monophyly and phylogenetic placement of the family Vaejovidae, sampling 17 new vaejovid libraries using high throughput transcriptomic sequencing. Our phylogenomic analyses revealed a previous misplacement of Smeringurus mesaensis. Regardless, we recovered Vaejovidae as diphyletic due to the placement of the enigmatic genus Uroctonus. The remaining vaejovids formed a clade that was strongly supported as the sister group of the superfamily Scorpionoidea, a placement insensitive to matrix completeness or concatenation vs. species tree approaches to inferring the tree topology. Chactoidea was invariably recovered as a paraphyletic group due to the nested placement of Scorpionoidea. As first steps to resolving the paraphyly of Chactoidea, we take the following systematic actions: (1) we establish the superfamily Superstitionoidea (new superfamily) to accommodate Superstitioniidae; (2) we restore Vaejovoidea (status revalidated) as a valid superfamily that excludes Uroctonus; and (3) we treat the families Caraboctonidae, Troglotayosicidae, and the subfamily Uroctoninae as incertae sedis with respect to superfamilial placement. Our systematic actions thus establish the monophyly of the presently redefined Chactoidea and Vaejovoidea.

The male sexual apparatus in the order Scorpiones (Arachnida): a comparative study of functional morphology as a tool to define hypotheses of homology.

BACKGROUND: Insemination in scorpions is carried out by means of a partly sclerotized structure, the spermatophore, which is composed of two separate halves, the hemispermatophores. In most genera these reproductive structures can be used to differentiate species. However, many taxa such as the genus Euscorpius and the family Diplocentridae lack the morphological diversity observed in the copulatory organs of many other arthropods, rendering them useless for species level taxonomy. Such structural stasis, however, suggests that hemispermatophores have evolved relatively slowly and may thus provide a stronger phylogenetic signal for recognizing supra-generic ranks than previously thought. Based on the postulate that the phenotypic stability observed in some groups is the consequence of functional constraint, the most comprehensive comparative study of the male sexual apparatus to date was conducted for a complete reassessment of the morphology, phylogenetic value and hypotheses of homology of these structures. RESULTS: Hemispermatophores, pre- and post-insemination spermatophores, as well as the inherent mechanisms of insemination, were studied across the whole order, allowing the recognition and description of a series of five basic bauplans for the capsular region. For the most part, these patterns appear to be consistent within each major taxonomic group, but several cases of incongruence between spermatophore morphology and taxonomy raises questions about the monophyly of some clades. The Bothriuridae are traditionally regarded as a basal scorpionoid family. However, except for the genus Lisposoma, bothriurid hemispermatophores and spermatophores are morphologically more similar to those of the Chactoidea than to those of scorpionoids. On the other hand, the male copulatory structures of the hormurid clade (Hormiops (Hormurus + Liocheles)) are more akin to those of Diplocentridae and Heteroscorpionidae than to those of other hormurids. CONCLUSIONS: Spermatophore capsular patterns appears to be congruent with a recent phylogeny of the order Scorpiones based on phylogenomic data that placed Bothriuridae outside of Scorpionoidea and Liocheles outside of Hormuridae, in contradicton with earlier phylogenetic reconstructions based on morphology. This raises questions about the potential use of functionally constrained traits to assess the reliability of contradicting phylogenetic hypotheses and emphasizes the need for a thorough reassessment of the scorpion phylogenetic relationships.

Evidence of duplicated Hox genes in the most recent common ancestor of extant scorpions.

Scorpions (order Scorpiones) are unusual among arthropods, both for the extreme heteronomy of their bauplan and for the high gene family turnover exhibited in their genomes. These phenomena appear to be correlated, as two scorpion species have been shown to possess nearly twice the number of Hox genes present in most arthropods. Segmentally offset anterior expression boundaries of a subset of Hox paralogs have been shown to correspond to transitions in segmental identities in the scorpion posterior tagmata, suggesting that posterior heteronomy in scorpions may have been achieved by neofunctionalization of Hox paralogs. However, both the first scorpion genome sequenced and the developmental genetic data are based on exemplars of Buthidae, one of 19 families of scorpions. It is therefore not known whether Hox paralogy is limited to Buthidae or widespread among scorpions. We surveyed 24 high throughput transcriptomes and the single whole genome available for scorpions, in order to test the prediction that Hox gene duplications are common to the order. We used gene tree parsimony to infer whether the paralogy was consistent with a duplication event in the scorpion common ancestor. Here we show that duplicated Hox genes in non-buthid scorpions occur in six of the ten Hox classes. Gene tree topologies and parsimony-based reconciliation of the gene trees are consistent with a duplication event in the most recent common ancestor of scorpions. These results suggest that a Hox paralogy, and by extension the model of posterior patterning established in a buthid, can be extended to non-Buthidae scorpions.

Phylogenomic resolution of scorpions reveals multilevel discordance with morphological phylogenetic signal.

Scorpions represent an iconic lineage of arthropods, historically renowned for their unique bauplan, ancient fossil record and venom potency. Yet, higher level relationships of scorpions, based exclusively on morphology, remain virtually untested, and no multilocus molecular phylogeny has been deployed heretofore towards assessing the basal tree topology. We applied a phylogenomic assessment to resolve scorpion phylogeny, for the first time, to our knowledge, sampling extensive molecular sequence data from all superfamilies and examining basal relationships with up to 5025 genes. Analyses of supermatrices as well as species tree approaches converged upon a robust basal topology of scorpions that is entirely at odds with traditional systematics and controverts previous understanding of scorpion evolutionary history. All analyses unanimously support a single origin of katoikogenic development, a form of parental investment wherein embryos are nurtured by direct connections to the parent's digestive system. Based on the phylogeny obtained herein, we propose the following systematic emendations: Caraboctonidae is transferred to Chactoidea new superfamilial assignment: ; superfamily Bothriuroidea revalidated: is resurrected and Bothriuridae transferred therein; and Chaerilida and Pseudochactida are synonymized with Buthida new parvordinal synonymies: .

Evidence for Eurogondwana: the roles of dispersal, extinction and vicariance in the evolution and biogeography of Indo-Pacific Hormuridae (Scorpiones: Scorpionoidea).

Scorpions previously assigned to the genus Liocheles Sundevall, 1883, of the family Hormuridae Laurie, 1896, are widely distributed in the tropical forests of the Indo-Pacific region. Revisionary systematics of these poorly known scorpions has revealed a tremendous diversity of species. As part of an ongoing investigation, the first analysis of Indo-Pacific hormurid scorpion phylogeny based on morphological data scored for all currently recognized species of Hormiops Fage, , Hormurus Thorell, 1876, and Liocheles, is presented. The taxonomy of these scorpions is reassessed and their biogeography reinterpreted in the light of the phylogeny. Phylogenetic, morphological, and distributional data support the revalidation of Hormiops and Hormurus, previously synonymized with Liocheles. The phylogeny indicates that the Australasian hormurids are more closely related to the Afrotropical and Neotropical hormurids than to the Indian hormurids, as previously proposed, refuting the "out-of-India" origin of Asian hormurids. A recent paleogeographical hypothesis, the "Eurogondwana model", is supported instead. According to this hypothesis, hormurid scorpions colonized Laurasia from Africa via the Apulia microplate (Europa terrane) in the Cretaceous, subsequently colonized the Australo-Papuan archipelago in the early-mid Cenozoic, and then went extinct in the Northern Hemisphere during the second half of the Cenozoic. These results suggest that, contrary to the traditional paradigm, dispersal and extinction may affect spatial and temporal biotic distributions as much as vicariance, even in animals with limited vagility, such as scorpions.

The genus Hormiops Fage, 1933 (Hormuridae, Scorpiones), a palaeoendemic of the South China Sea: systematics and biogeography.

The monotypic genus Hormiops Fage, 1933 is so far only known from two groups of granitic islands off the coasts of Peninsular Malaysia and Vietnam. Examination of newly collected material from both archipelagos and of the type series of Hormiops davidovi Fage, 1933 reveals previously disregarded morphological differences sufficient to assign the Malaysian specimens to a distinct species, described here as Hormiops infulcra sp. nov. An updated diagnosis of the genus, as well as a dichotomic key enabling the determination of Hormiops from its close relatives, Hormurus Thorell, 1876 and Liocheles Sundevall, 1833 are also provided. The phylogenetic position, distribution pattern, and ecology of these insular scorpions suggest that they are palaeoendemics, remnants of a previously more widely distributed lineage. A biogeographical model is proposed for the genus based on these observations and on a synthesis of palaeogeographical and palaeoenvironmental data currently available for Sundaland.