Hox genes and the phylogeny of the arthropods

The arthropods are the most speciose, and among the most morphologically diverse, of the animal phyla. Their evolution has been the subject of intense research for well over a century, yet the relationships among the four extant arthropod subphyla - chelicerates, crustaceans, hexapods, and myriapods - are still not fully resolved. Morphological taxonomies have often placed hexapods and myriapods together (the Atelocerata) [1, 2], but recent molecular studies have generally supported a hexapod/crustacean clade [2-9]. A cluster of regulatory genes, the Hox genes, control segment identity in arthropods, and comparisons of the sequences and functions of Hox genes can reveal evolutionary relationships [10]. We used Hox gene sequences from a range of arthropod taxa, including new data from a basal hexapod and a myriapod, to estimate a phylogeny of the arthropods. Our data support the hypothesis that insects and crustaceans form a single clade within the arthropods to the exclusion of myriapods. They also suggest that myriapods are more closely allied to the chelicerates than to this insect/crustacean clade.     

The cuticle of the enigmatic arthropod Phytophilaspis and biomineralization in Cambrian arthropods

Lin, J.‐P., Ivantsov, A.Y. & Briggs, D.E.G. 2011: The cuticle of the enigmatic arthropod Phytophilaspis and biomineralization in Cambrian arthropods. Lethaia, Vol. 44, pp. 344–349. Many non‐trilobite arthropods occur in Cambrian Burgess Shale‐type (BST) biotas, but most of these are preserved in fine‐grained siliciclastics. Only one important occurrence of Cambrian non‐trilobite arthropods, the Sinsk biota (lower Sinsk Formation, Botomian) from the Siberian Platform, has been discovered in carbonates. The chemical compositions of samples of the enigmatic arthropod Phytophilaspis pergamena Ivantsov, 1999 and the co‐occurring trilobite Jakutus primigenius Ivantsov in Ponomarenko, 2005 from this deposit were analysed. The cuticle of P. pergamena is composed of mainly calcium phosphate and differs from the cuticle of J. primigenius, which contains only calcium carbonate. Phosphatized cuticles are rare among large Cambrian arthropods, except for aglaspidids and a few trilobites. Based on recent phylogenetic studies, phosphatization of arthropod cuticle is likely to have evolved several times. □arthropod cuticle, Burgess Shale‐type preservation, fossil‐diagenesis, phosphatization.     

Arthropod phylogeny: An overview from the perspectives of morphology,molecular data and the fossil record

Monophyly of Arthropoda is emphatically supported from both morphological and molecular perspectives. Recent work finds Onychophora rather than Tardigrada to be the closest relatives of arthropods. The status of tardigrades as panarthropods (rather than cycloneuralians) is contentious from the perspective of phylogenomic data. A grade of Cambrian taxa in the arthropod stem group includes gilled lobopodians, dinocaridids (e.g., anomalocaridids), fuxianhuiids and canadaspidids that inform on character acquisition between Onychophora and the arthropod crown group. A sister group relationship between Crustacea (itself likely paraphyletic) and Hexapoda is retrieved by diverse kinds of molecular data and is well supported by neuroanatomy. This clade, Tetraconata, can be dated to the early Cambrian by crown group-type mandibles. The rival Atelocerata hypothesis (Myriapoda + Hexapoda) has no molecular support. The basal node in the arthropod crown group is embroiled in a controversy over whether myriapods unite with chelicerates (Paradoxopoda or Myriochelata) or with crustaceans and hexapods (Mandibulata). Both groups find some molecular and morphological support, though Mandibulata is presently the stronger morphological hypothesis. Either hypothesis forces an unsampled ghost lineage for Myriapoda from the Cambrian to the mid Silurian.     

An Early Devonian arthropod fauna from the Windyfield cherts, Aberdeenshire, Scotland

New terrestrial and freshwater arthropods are described from the Windyfield cherts, a suite of silicified sinters deposited 700m north‐east of the Rhynie cherts and part of the same Early Devonian hot‐spring complex. The diverse assemblage consists of Heterocrania rhyniensis (Hirst and Maulik, 1926a), here recognized as a euthycarcinoid; scutigeromorph centipede material assigned to Crussolum sp.; the crustacean Lepidocaris; trigonotarbid arachnids; a new arthropod of myriapod affinities named Leverhulmia mariae gen. et sp. nov.; and the distinctively ornamented arthropod cuticle of Rhynimonstrum dunlopi gen. et sp. nov. The Leverhulmia animal preserves gut content identifying it as an early terrestrial detritivore. Abundant coprolites of similar composition and morphology to the gut contents of the euthycarcinoid crowd the matrix. Chert texture, faunal associations, and study of modern analogues strongly suggest that the terrestrial arthropods were ubiquitous Early Devonian forms with no particular special adaptation to localized conditions around the terrestrial hot‐spring vents. The aquatic arthropods represent biota from ephemeral cool‐water pools in the vicinity of the hot‐spring vents.     

The geological record and phylogeny of the Myriapoda

We review issues of myriapod phylogeny, from the position of the Myriapoda amongst arthropods to the relationships of the orders of the classes Chilopoda and Diplopoda. The fossil record of each myriapod class is reviewed, with an emphasis on developments since 1997. We accept as working hypotheses that Myriapoda is monophyletic and belongs in Mandibulata, that the classes of Myriapoda are monophyletic, and that they are related as (Chilopoda (Symphyla (Diplopoda + Pauropoda))). The most pressing challenges to these hypotheses are some molecular and developmental evidence for an alliance between myriapods and chelicerates, and the attraction of symphylans to pauropods in some molecular analyses. While the phylogeny of the orders of Chilopoda appears settled, the relationships within Diplopoda remain unclear at several levels. Chilopoda and Diplopoda have a relatively sparse representation as fossils, and Symphyla and Pauropoda fossils are known only from Tertiary ambers. Fossils are difficult to place in trees based on living forms because many morphological characters are not very likely to be preserved in the fossils; as a consequence, most diplopod fossils have been placed in extinct higher taxa. Nevertheless, important information from diplopod fossils includes the first documented occurrence of air-breathing, and the first evidence for the use of a chemical defense. Stem-group myriapods are unknown, but evidence suggests the group must have arisen in the Early Cambrian, with a major period of cladogenesis in the Late Ordovician and early Silurian. Large terrestrial myriapods were on land at least by mid-Silurian.     

Gene expression suggests conserved mechanisms patterning the heads of insects and myriapods

Segmentation, i.e. the subdivision of the body into serially homologous units, is one of the hallmarks of the arthropods. Arthropod segmentation is best understood in the fly Drosophila melanogaster. But different from the situation in most arthropods in this species all segments are formed from the early blastoderm (so called long-germ developmental mode). In most other arthropods only the anterior segments are formed in a similar way (so called short-germ developmental mode). Posterior segments are added one at a time or in pairs of two from a posterior segment addition zone. The segmentation mechanisms are not universally conserved among arthropods and only little is known about the genetic patterning of the anterior segments. Here we present the expression patterns of the insect head patterning gene orthologs hunchback (hb), orthodenticle (otd), buttonhead-like (btdl), collier (col), cap-n-collar (cnc) and crocodile (croc), and the trunk gap gene Krüppel (Kr) in the myriapod Glomeris marginata. Conserved expression of these genes in insects and a myriapod suggests that the anterior segmentation system may be conserved in at least these two classes of arthropods. This finding implies that the anterior patterning mechanism already existed in the last common ancestor of insects and myriapods.     

The phylogeny of aglaspidid arthropods and the internal relationships within Artiopoda

The phylogenetic position of aglaspidids, a problematic group of Lower Palaeozoic arthropods of undetermined affinities, is re‐examined in the context of the major Cambrian and Ordovician lamellipedian arthropod groups. A cladistic analysis of ten genera of aglaspidids sensu stricto, six aglaspidid‐like arthropods and 42 Palaeozoic arthropod taxa indicates that Xenopoda, Cheloniellida, Aglaspidida sensu lato and Trilobitomorpha form a clade (Artiopoda Hou and Bergström, 1997 ) nested within the mandibulate stem‐lineage, thus discarding previous interpretations of these taxa as part 'of the chelicerate stem‐group (Arachnomorpha Heider, 1913 ). The results confirm an aglaspidid identity for several recently described arthropods, including Quasimodaspis brentsae, Tremaglaspis unite, Chlupacaris dubia, Australaglaspis stonyensis and an unnamed Ordovician Chinese arthropod. The problematic Bohemian arthropod Kodymirus vagans was recovered as sister taxon to Beckwithia typa, and both form a small clade that falls outside Aglaspidida sensu stricto, thus discarding eurypterid affinities for the former. The analysis does not support the phylogenetic position of Kwanyinaspis maotianshanensis at the base of Conciliterga as proposed in recent studies, but rather occupies a basal position within Aglaspidida sensu lato. The results indicate a close association of aglaspidid arthropods with xenopods (i.e. Emeraldella and Sidneyia) and cheloniellids (e.g. Cheloniellon, Duslia); the new clade “Vicissicaudata” is proposed to encompass these arthropods, which are characterized by a differentiated posterior region. The phylogenetic position of aglaspidid arthropods makes them good outgroup candidates for analysing the internal relationships within the groups that form Trilobitomorpha. This work provides a much clearer picture of the phylogenetic relationships among Lower Palaeozoic lamellipedians.     

A New Bivalved Arthropod from the Early Cambrian Sirius Passet Fauna, North Greenland

A new bivalved arthropod is described from the Lower Cambrian (?Upper Atdabanian) Buen Formation of North Greenland. Pauloterminus spinodorsalis gen. et sp. nov. possesses a bivalved carapace that covers the head, which has a single pair of antennae, and anteriormost thorax. No mouthparts are visible. The five‐segmented abdomen was limbless and terminated in a telson plus a pair of large, lobate uropods. A suite of at least six biramous thoracic limbs are present: the short endopods are made up of small, serial podomeres, while the exopods are lobate and may have functioned as gills as well as in swimming. Partially infilled guts are occasionally visible, suggesting that this animal may have been a sediment feeder. It is compared to other Cambrian bivalved arthropods, especially the waptiids Chuandianella ovata from the Lower Cambrian Chengjiang fauna (China) and Waptia fieldensis from the Middle Cambrian Burgess Shale (British Columbia). Of these three animals, the Greenland and Chinese taxa appear to be the most closely related. P. spinodorsalis possesses many typical arthropod features, but it also demonstrates more primitive characters that are more reminiscent of the lobopodians.     

A forgotten homology supporting the monophyly of Tracheata: The subcoxa of insects and myriapods re-visited

The current discussion about the relationships of higher arthropod taxa has led to a conflict between the traditional Tracheata (=Atelocerata) concept (hexapods united with myriapods), the Tetraconata concept (hexapods united with crustaceans, excluding myriapods), and the Paradoxopoda or Myriochelata concept (myriapods united with cheliceratans), with major contradictions between morphological and molecular data. We have analyzed a character set which apparently has completely vanished from the recent debate, namely the equipment of the trunk pleura of myriapods and insects with a characteristic set of concentric sclerites around the leg base and accompanying muscles. Based on the work of Heymons (1899) these sclerites were thought to be remains of the first appendage article, then denominated “subcoxa”. We have re-visited this old idea and show the arrangement of the much discussed pleural structures by SEM for the first time. Obviously a characteristic pattern of concentric pleural plates around the leg-base is present in all major myriapod taxa, including for the first time evidence for their presence in Progoneata. Because of their equal structure and orientation, the pleural sclerites present in entognathous and ectognathous insects may be derived from the same ground pattern. We conclude that the pleurites of Hexapoda and Myriapoda seem to be homologous structures, and there is evidence that the “subcoxa” of Tracheata is homologous with the coxa of crustaceans. Since no other arthropods show these sclerites, the transformation of the crustacean coxa to the pleural region in myriapods and insects is probably a synapomorphy congruent with the traditional Tracheata-hypothesis. Further investigations of recently published molecular work using the phylogenetic network software SplitsTree V.4 indicate that information content of several data sets is not convincing.     

Reconsideration of the supposed naraoiid larva from the Early Cambrian Chengjiang Lagerstätte, South China

The Chengjiang Lagerstätte in the Lower Cambrian of South China yields a small, larva‐like arthropod, which was considered to be a protaspis of naraoiids by many authors. The discovery of a large number of well‐preserved specimens from many new localities has allowed the original study to be revised. The relatively large size, stable morphology and unusual structure of the appendages indicate that these specimens represent adults of a new arthropod, Primicaris larvaformis. The larva‐like outline is considered to have arisen by the heterochronic process of progenesis. In addition, this animal displays primitive aspects of bodyplan and limb morphology that suggest a basal position within arachnomorphs, or perhaps even arthropods, and the similarities to the Vendian arthropod‐like animal Parvancorina probably provide an evolutionary link between Vendian forms and Cambrian arthropods.     

Neurogenesis in myriapods and chelicerates and its importance for understanding arthropod relationships

Several alternative hypotheses on the relationships betweenthe major arthropod groups are still being discussed. We reexaminehere the chelicerate/myriapod relationship by comparing previouslypublished morphological data on neurogenesis in the euarthropodgroups and presenting data on an additional myriapod (Strigamiamaritima). Although there are differences in the formation ofneural precursors, most euarthropod species analyzed generateabout 30 single neural precursors (insects/crustaceans) or precursorgroups (chelicerates/myriapods) per hemisegment that are arrangedin a regular pattern. The genetic network involved in recruitmentand specification of neural precursors seems to be conservedamong euarthropods. Furthermore, we show here that neural precursoridentity seems to be achieved in a similar way. Besides theseconserved features we found 2 characters that distinguish insects/crustaceansfrom myriapods/chelicerates. First, in insects and crustaceansthe neuroectoderm gives rise to epidermal and neural cells,whereas in chelicerates and myriapods the central area of theneuroectoderm exclusively generates neural cells. Second, neuralcells arise by stem-cell-like divisions of neuroblasts in insectsand crustaceans, whereas groups of mainly postmitotic neuralprecursors are recruited for the neural fate in cheliceratesand myriapods. We discuss whether these characteristics representa sympleisiomorphy of myriapods and chelicerates that has beenlost in the more derived Pancrustacea or whether these characteristicsare a synapomorphy of myriapods and chelicerates, providingthe first morphological support for the Myriochelata group.     

A rare non‐trilobite artiopodan from the Guzhangian (Cambrian Series 3) Weeks Formation Konservat‐Lagerstätte in Utah,USA

We describe a weakly biomineralized non‐trilobite artiopodan arthropod from the Guzhangian Weeks Formation of Utah. Falcatamacaris bellua gen. et sp. nov. is typified by a thin calcitic cuticle, broad cephalon without eyes or dorsal ecdysial sutures, an elongate trunk with distinctively sickle‐shaped pleural spines and a long tailspine with a bifurcate termination. The precise affinities of Falcatamacaris gen. nov. are problematic due to the presence of unique features within Artiopoda, such as the peculiar morphology of the pleural and posterior regions of the trunk. Possible affinities with aglaspidid‐like arthropods and concilitergans are discussed based on the possession of 11 trunk tergites, edge‐to‐edge articulations and overall body spinosity. The new taxon highlights the importance of the Weeks Formation Konservat‐Lagerstätte for further understanding the diversity of extinct arthropod groups in the upper Cambrian.     

A Parvancorina-like arthropod from the Cambrian of South China

Constraining the origin of animal groups is allowed, to some extent, by discoveries of Cambrian Lagerstätten that preserve both mineralizing and nonmineralizing organisms. A new species is reported here of the Cambrian arthropod Skania, which bears an exoskeleton that shares homologies with the Neoproterozoic (Ediacaran) organism Parvancorina and firmly establishes a Precambrian root for arthropods. A new monophyletic group, Parvancorinomorpha, is proposed as the first clade within the arthropod crown group demonstrably ranging across the Neoproterozoic–Paleozoic transition. The Parvancorinomorpha is interpreted to be the sister group of the Arachnomorpha. Incipient cephalization in Skania and related genera represents a step in the progression toward division of a cephalon from a large posterior trunk as shown in Cambrian arachnomorphs such as naraoiids and the addition of a pygidium and thoracic tergites as shown in the arachnomorph clade basal to trilobites. This evidence can serve as a new calibration point for estimating the divergence time for the last common ancestor of arthropods and priapulids based on molecular clock methods.     

Cambrocaris baltica n. gen. n. sp., a possible stem-lineage crustacean from the Upper Cambrian of Poland

Bodily preserved, secondarily phosphatized arthropods discovered in drill cores on He***l Peninsula, northern Poland, and in its vicinity date from the Upper Cambrian. Comparisons between a group of arthropods of the Upper Cambrian of Sweden recognized as stem-lineage crustaceans indicate that one of these new forms, Cambrocaris baltica n. gen. n. sp., also represents a derivative of the early phase of crustacean evolution prior to the crown-group level. The material also yielded a specimen identified as Skara minuta Müller & Walossek, 1985, hitherto known only from Västergotland, Sweden, and two limb fragments which cannot be assigned to species. □ Crustacea, stem-lineage derivatives. Phosphatization, three-dimensional preservation, Upper Cambrian, Alum shales, 'Orsten', northern Poland.     

Expression of the decapentaplegic ortholog in embryos of the onychophoran Euperipatoides rowelli

The gene decapentaplegic (dpp) and its homologs are essential for establishing the dorsoventral body axis in arthropods and vertebrates. However, the expression of dpp is not uniform among different arthropod groups. While this gene is expressed along the dorsal body region in insects, its expression occurs in a mesenchymal group of cells called cumulus in the early spider embryo. A cumulus-like structure has also been reported from centipedes, suggesting that it might be either an ancestral feature of arthropods or a derived feature (=synapomorphy) uniting the chelicerates and myriapods. To decide between these two alternatives, we analysed the expression patterns of a dpp ortholog in a representative of one of the closest arthropod relatives, the onychophoran Euperipatoides rowelli. Our data revealed unique expression patterns in the early mesoderm anlagen of the antennal segment and in the dorsal and ventral extra-embryonic tissue, suggesting a divergent role of dpp in these tissues in Onychophora. In contrast, the expression of dpp in the dorsal limb portions resembles that in arthropods, except that it occurs in the mesoderm rather than in the ectoderm of the onychophoran limbs. A careful inspection of embryos of E. rowelli revealed no cumulus-like accumulation of dpp expressing cells at any developmental stage, suggesting that this feature is either a derived feature of chelicerates or a synapomorphy uniting the chelicerates and myriapods.     

Expression of the decapentaplegic ortholog in embryos of the onychophoran Euperipatoides rowelli

The gene decapentaplegic (dpp) and its homologs are essential for establishing the dorsoventral body axis in arthropods and vertebrates. However, the expression of dpp is not uniform among different arthropod groups. While this gene is expressed along the dorsal body region in insects, its expression occurs in a mesenchymal group of cells called cumulus in the early spider embryo. A cumulus-like structure has also been reported from centipedes, suggesting that it might be either an ancestral feature of arthropods or a derived feature (=synapomorphy) uniting the chelicerates and myriapods. To decide between these two alternatives, we analysed the expression patterns of a dpp ortholog in a representative of one of the closest arthropod relatives, the onychophoran Euperipatoides rowelli. Our data revealed unique expression patterns in the early mesoderm anlagen of the antennal segment and in the dorsal and ventral extra-embryonic tissue, suggesting a divergent role of dpp in these tissues in Onychophora. In contrast, the expression of dpp in the dorsal limb portions resembles that in arthropods, except that it occurs in the mesoderm rather than in the ectoderm of the onychophoran limbs. A careful inspection of embryos of E. rowelli revealed no cumulus-like accumulation of dpp expressing cells at any developmental stage, suggesting that this feature is either a derived feature of chelicerates or a synapomorphy uniting the chelicerates and myriapods.     

A phylogenetic analysis of Myriapoda (Arthropoda) using two nuclear protein-encoding genes

Nucleotide and inferred amino acid sequences from two nuclear protein-encoding genes, elongation factor-aα and RNA polymerase II, were obtained from 34 myriapods and 14 other arthropods to determine phylogenetic relationships among and within the myriapod classes. Phylogenetic analyses using maximum parsimony and maximum likelihood methods recovered all three represented myriapod classes (Chilopoda, Diplopoda, Symphyla) and all multiply sampled chilopod and diplopod orders, often with high node support. In contrast, relationships between classes and between orders were recovered less consistently and node support was typically lower. The temporal structure of phylogenetic diversification in Myriapoda may explain this apparent pattern of the phylogenetic recovery.     

Neurogenesis in the chilopod <Emphasis Type="Italic">Lithobius forficatus</Emphasis> suggests more similarities to chelicerates than to insects

In a recent comparative study on neurogenesis in the diplopod Glomeris marginata we have shown that the millipede and the spider share several features that cannot be found in homologous form in insects and crustaceans. The most distinctive difference is that groups of neural precursors are singled out from the neuroectoderm of the spider and the diplopod, rather than individual cells (i.e. neuroblasts) as in insects or crustacean. This observation constitutes the first morphological indication for a close myriapod/chelicerate relationship that has otherwise only been suggested by molecular phylogenetic analysis. To see whether the pattern of neurogenesis described for the diplopod is representative for myriapods, we analysed neurogenesis in the basal chilopod Lithobius forficatus. We show here that groups of cells invaginate from the chilopod neuroectoderm at strikingly similar positions as the invaginating cell groups of the diplopod and the spider. Furthermore, the expression patterns of the proneural and neurogenic genes reveal more similarities to the chelicerate and the diplopod than to insects. Thus, chelicerates and myriapods share the developmental mechanism for neurogenesis, either because they are true sister groups, or because this reflects the ancestral state of neurogenesis in arthropods.Edited by P. Simpson     

MORE THAN ONE WAY TO PRODUCE PROTEIN DIVERSITY: DUPLICATION AND LIMITED ALTERNATIVE SPLICING OF AN ADHESION MOLECULE GENE IN BASAL ARTHROPODS

Exon duplication and alternative splicing evolved multiple times in metazoa and are of overall importance in shaping genomes and allowing organisms to produce many fold more proteins than there are genes in the genome. No other example is as striking as the one of the Down syndrome cell adhesion molecule (Dscam) of insects and crustaceans (pancrustaceans) involved in the nervous system differentiation and in the immune system. To elucidate the evolutionary history of this extraordinary gene, we investigated Dscam homologs in two basal arthropods, the myriapod Strigamia maritima and the chelicerate Ixodes scapularis. In both, Dscam diversified extensively by whole gene duplications resulting in multigene expansions. Within some of the S. maritima genes, exons coding for one of the immunoglobulin domains (Ig7) duplicated and are mutually exclusively alternatively spliced. Our results suggest that Dscam diversification was selected independently in chelicerates, myriapods, and pancrustaceans and that the usage of Dscam diversity by immune cells evolved for the first time in basal arthropods. We propose an evolutionary scenario for the appearance of the highly variable Dscam gene of pancrustaceans, adding to the understanding of how alternative splicing, exon, and gene duplication contribute to create molecular diversity associated with potentially new cellular functions.     

Cephalic and appendage morphology of the Cambrian arthropod Sidneyia inexpectans

Sidneyia inexpectans Walcott, 1911 from the Cambrian Series 3 Burgess Shale of British Columbia is largely accepted as a representative of the artiopodans, an assemblage of Paleozoic arthropod taxa, including trilobites and their immediate relatives. Its appendage morphology was never fully understood, but the exopod seemed to differ from that of other artiopodans, except for the shared presence of lamellae. The head was considered to comprise only the ocular and antennular segments, these being covered entirely on the ventral side by a large doublure. This short head was often taken as an evidence for variability of head segment counts in Cambrian arthropods, and to falsify the hypothesis of a head with three postantennular segments in the euarthropod ground pattern. Restudy of a substantial amount of material of S. inexpectans shows that previous interpretations of a short head were based on taphonomically deformed specimens, where the head was either partly folded, or entirely flipped under the thorax, resulting in the dorsal shield being mistaken for an extensive doublure. Rather than an extensive doublure, there is a broad hypostome, and the head comprises ocular, antennular, and at least two postantennular appendage bearing segments. The appendage morphology is shown to be consistent with artiopodan affinities. The exopod is of the bilobate flap-like type with lamellae inserting on the proximal portion, earlier proposed as a potential autapomorphy of Artiopoda. Reinforcement of artiopodan affinities for S. inexpectans and reinterpretation of its head reconciles this species with current understanding of arthropod phylogeny and head segmentation.