BackgroundTransposable elements (TEs) are a major component of metazoan genomes and are associated with a variety of mechanisms that shape genome architecture and evolution. Despite the ever-growing number of insect genomes sequenced to date, our understanding of the diversity and evolution of insect TEs remains poor.ResultsHere, we present a standardized characterization and an order-level comparison of arthropod TE repertoires, encompassing 62 insect and 11 outgroup species. The insect TE repertoire contains TEs of almost every class previously described, and in some cases even TEs previously reported only from vertebrates and plants. Additionally, we identified a large fraction of unclassifiable TEs. We found high variation in TE content, ranging from less than 6% in the antarctic midge (Diptera), the honey bee and the turnip sawfly (Hymenoptera) to more than 58% in the malaria mosquito (Diptera) and the migratory locust (Orthoptera), and a possible relationship between the content and diversity of TEs and the genome size.ConclusionWhile most insect orders exhibit a characteristic TE composition, we also observed intraordinal differences, e.g., in Diptera, Hymenoptera, and Hemiptera. Our findings shed light on common patterns and reveal lineage-specific differences in content and evolution of TEs in insects. We anticipate our study to provide the basis for future comparative research on the insect TE repertoire.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1324-9) contains supplementary material, which is available to authorized users.
Velvet worms eject a fluid capture slime that can be mechanically drawn into stiff biopolymeric fibres. Remarkably, these fibres can be dissolved by extended exposure to water, and new regenerated fibres can be drawn from the dissolved fibre solution—indicating a fully recyclable process. Here, we perform a multiscale structural and compositional investigation of this reversible fabrication process with the velvet worm Euperipatoides rowelli, revealing that biopolymeric fibre assembly is facilitated via mono-disperse lipid-protein nanoglobules. Shear forces cause nanoglobules to self-assemble into nano- and microfibrils, which can be drawn into macroscopic fibres with a protein-enriched core and lipid-rich coating. Fibre dissolution in water leads to re-formation of nanoglobules, suggesting that this dynamic supramolecular assembly of mechanoresponsive protein-building blocks is mediated by reversible non-covalent interactions. These findings offer important mechanistic insights into the role of mechanochemical processes in bio-fibre formation, providing potential avenues for sustainable material fabrication processes.
BackgroundWhile recent neuroanatomical and gene expression studies have clarified the alignment of cephalic segments in arthropods and onychophorans, the identity of head segments in tardigrades remains controversial. In particular, it is unclear whether the tardigrade head and its enclosed brain comprises one, or several segments, or a non-segmental structure. To clarify this, we applied a variety of histochemical and immunocytochemical markers to specimens of the tardigrade Macrobiotus cf. harmsworthi and the onychophoran Euperipatoides rowelli.Methodology/Principal FindingsOur immunolabelling against serotonin, FMRFamide and α-tubulin reveals that the tardigrade brain is a dorsal, bilaterally symmetric structure that resembles the brain of onychophorans and arthropods rather than a circumoesophageal ring typical of cycloneuralians (nematodes and allies). A suboesophageal ganglion is clearly lacking. Our data further reveal a hitherto unknown, unpaired stomatogastric ganglion in Macrobiotus cf. harmsworthi, which innervates the ectodermal oesophagus and the endodermal midgut and is associated with the second leg-bearing segment. In contrast, the oesophagus of the onychophoran E. rowelli possesses no immunoreactive neurons, whereas scattered bipolar, serotonin-like immunoreactive cell bodies are found in the midgut wall. Furthermore, our results show that the onychophoran pharynx is innervated by a medullary loop nerve accompanied by monopolar, serotonin-like immunoreactive cell bodies.Conclusions/SignificanceA comparison of the nervous system innervating the foregut and midgut structures in tardigrades and onychophorans to that of arthropods indicates that the stomatogastric ganglion is a potential synapomorphy of Tardigrada and Arthropoda. Its association with the second leg-bearing segment in tardigrades suggests that the second trunk ganglion is a homologue of the arthropod tritocerebrum, whereas the first ganglion corresponds to the deutocerebrum. We therefore conclude that the tardigrade brain consists of a single segmental region corresponding to the arthropod protocerebrum and, accordingly, that the tardigrade head is a non-composite, one-segmented structure.
A fundamental question in biology is how animal segmentation arose during evolution. One particular challenge is to clarify whether segmental ganglia of the nervous system evolved once, twice, or several times within the Bilateria. As close relatives of arthropods, Onychophora play an important role in this debate since their nervous system displays a mixture of both segmental and non-segmental features. We present evidence that the onychophoran "ventral organs," previously interpreted as segmental anlagen of the nervous system, do not contribute to nerve cord formation and therefore cannot be regarded as vestiges of segmental ganglia. The early axonal pathways in the central nervous system arise by an anterior-to-posterior cascade of axonogenesis from neuronal cell bodies, which are distributed irregularly along each presumptive ventral cord. This pattern contrasts with the strictly segmental neuromeres present in arthropod embryos and makes the assumption of a secondary loss of segmentation in the nervous system during the evolution of the Onychophora less plausible. We discuss the implications of these findings for the evolution of neural segmentation in the Panarthropoda (Arthropoda+Onychophora+Tardigrada). Our data best support the hypothesis that the ancestral panarthropod had only a partially segmented nervous system, which evolved progressively into the segmental chain of ganglia seen in extant tardigrades and arthropods.
BackgroundAlthough molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods. To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. In addition, we performed retrograde staining of nerves in the onychophoran Euperipatoides rowelli in order to compare the serial locations of motor neurons within the nervous system relative to the appendages they serve in arthropods, tardigrades and onychophorans.ResultsContrary to a previous report from a Macrobiotus species, our immunocytochemical and electron microscopic data revealed contralateral fibres and bundles of neurites in each trunk ganglion of three tardigrade species, including Macrobiotus cf. harmsworthi, Paramacrobiotus richtersi and Hypsibius dujardini. Moreover, we identified additional, extra-ganglionic commissures in the interpedal regions bridging the paired longitudinal connectives. Within the ganglia we found serially repeated sets of serotonin- and RFamid-like immunoreactive neurons. Furthermore, our data show that the trunk ganglia of tardigrades, which include the somata of motor neurons, are shifted anteriorly with respect to each corresponding leg pair, whereas no such shift is evident in the arrangement of motor neurons in the onychophoran nerve cords.ConclusionsTaken together, these data reveal three major correspondences between the segmental ganglia of tardigrades and arthropods, including (i) contralateral projections and commissures in each ganglion, (ii) segmentally repeated sets of immunoreactive neurons, and (iii) an anteriorly shifted (parasegmental) position of ganglia. These correspondences support the homology of segmental ganglia in tardigrades and arthropods, suggesting that these structures were either lost in Onychophora or, alternatively, evolved in the tardigrade/arthropod lineage.
The current distributions of widespread groups of terrestrial animals and plants are supposedly the result of a mixture of either vicariance owing to continental split or more recent trans-oceanic dispersal. For organisms exhibiting a vicariant biogeographic pattern-achieving their current distribution by riding on the plates of former supercontinents-this view is largely inspired by the belief that Pangaea lacked geographical or ecological barriers, or that extinctions and dispersal would have erased any biogeographic signal since the early Mesozoic. We here present a time-calibrated molecular phylogeny of Onychophora (velvet worms), an ancient and exclusively terrestrial panarthropod group distributed throughout former Pangaean landmasses. Our data not only demonstrate that trans-oceanic dispersal does not need be invoked to explain contemporary distributions, but also reveal that the early diversification of the group pre-dates the break-up of Pangaea, maintaining regionalization even in landmasses that have remained contiguous throughout the history of the group. These results corroborate a growing body of evidence from palaeontology, palaeogeography and palaeoclimatic modelling depicting ancient biogeographic regionalization over the continuous landmass of Pangaea.
Background:Arthropods comprise the largest and most diverse phylum on Earth and play vital roles in nearly every ecosystem. Their diversity stems in part from variations on a conserved body plan, resulting from and recorded in adaptive changes in the genome. Dissection of the genomic record of sequence change enables broad questions regarding genome evolution to be addressed, even across hyper-diverse taxa within arthropods. Results:Using 76 whole genome sequences representing 21 orders spanning more than 500 million years of arthropod evolution, we document changes in gene and protein domain content and provide temporal and phylogenetic context for interpreting these innovations. We identify many novel gene families that arose early in the evolution of arthropods and during the diversification of insects into modern orders. We reveal unexpected variation in patterns of DNA methylation across arthropods and examples of gene family and protein domain evolution coincident with the appearance of notable phenotypic and physiological adaptations such as flight, metamorphosis, sociality and chemoperception. Conclusions:These analyses demonstrate how large-scale comparative genomics can provide broad new insights into the genotype to phenotype map and generate testable hypotheses about the evolution of animal diversity.
Screening of a deeply sequenced transcriptome using Illumina sequencing as well as the genome of the tardigrade Hypsibius dujardini revealed a set of five opsin genes. To clarify the phylogenetic position of these genes and to elucidate the evolutionary history of opsins in Panarthropoda (Onychophora + Tardigrada + Arthropoda), we reconstructed the phylogeny of broadly sampled metazoan opsin genes using maximum likelihood and Bayesian inference methods in conjunction with carefully selected substitution models. According to our findings, the opsin repertoire of H. dujardini comprises representatives of all three major bilaterian opsin clades, including one r-opsin, three c-opsins, and a Group 4 opsin (neuropsin/opsin-5). The identification of the tardigrade ortholog of neuropsin/opsin-5 is the first record of this opsin type in a protostome, but our screening of available metazoan genomes revealed that it is also present in other protostomes. Our opsin phylogeny further suggests that two r-opsins, including an “arthropsin,” were present in the last common ancestor of Panarthropoda. Although both r-opsin lineages were retained in Onychophora and Arthropoda, the arthropsin was lost in Tardigrada. The single (most likely visual) r-opsin found in H. dujardini supports the hypothesis of monochromatic vision in the panarthropod ancestor, whereas two duplications of the ancestral panarthropod c-opsin have led to three c-opsins in tardigrades. Although the early-branching nodes are unstable within the metazoans, our findings suggest that the last common ancestor of Bilateria possessed six opsins: Two r-opsins, one c-opsin, and three Group 4 opsins, one of which (Go opsin) was lost in the ecdysozoan lineage.
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