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Few fossils demonstrate the presence of the Hemichordata (Enteropneusta, Pterobranchia – excluding benthic and planktic Graptolithina) in the early Palaeozoic. Many of these early records are questionable and are not supported by a reliable fossil record. First definitive fossils are found in the Fortunian (early Cambrian) with the record of Sokoloviina representing fragments of the tubarium of the Pterobranchia. Possible Enteropneusta have been described from the Miaolingian (Wuliuan) and the slightly older Cambrian Series 2, Stage 3, but the record is largely based on poor inconclusive material. However, the Fortunian pterobranchs clearly indicate that a differentiation of the Enteropneusta and Pterobranchia must have happened earlier, even though a definitive fossil record is not available. The evolutionary origin of the Hemichordata (Enteropneusta & Pterobranchia), thus is likely to be found in the latest Ediacaran. Fossil burrows of Gyrolithes spp. at the Ediacaran–Cambrian GSSP may represent the activity of Enteropneusta, but cannot demonstrate without doubt their presence. Difficult is also the interpretation of meandering deep-water feeding traces or faecal traces in the Cambrian (cf. Nereites ichnofacies) that are similar to those produced by extant Enteropneusta (Torquaratoridae). The possible erect housing construction identified as Margaretia is unlikely to be built by an enteropneust and is not comparable in any way with the organic-walled tubarium constructions of the Pterobranchia. [ABSTRACT FROM AUTHOR]

Worm-like endosymbionts were found in the hepatic region of the digestive tract of the deep-sea acorn worm Quatuoralisia malakhovi Ezhova et Lukinykh, 2022 (family Torquaratoridae) from the Bering Sea. The symbionts were assigned to the taxon Nemertodermatida on the basis of histological examination. Torquaratoridae are similar in feeding type to holothuroids, which have also been found to have Xenacoelomorpha endosymbionts. [ABSTRACT FROM AUTHOR]

Abstract Schizocardium karankawa sp. nov. has been collected from subtidal muds of the Laguna Madre, Texas, and the Mississippi coast, Gulf of Mexico. The Texas population is reproductive from early February to mid-April. Gametes are liberated by a small incision in a gonad. Oocyte germinal vesicle breakdown is increased in the presence of sperm, and the highest fertilization success was in the artificial seawater Jamarin U. Manually dechorionated embryos develop normally. Development was asynchronous via a tornaria larva, metamorphosis and maintained to the juvenile worm 6 gill-pore stage. Phalloidin-labeled late-stage tornaria revealed retractor muscles that connect the pericardial sac with the apical tuft anteriorly, the oesophagus ventrally, and muscle cells of the early mesocoels. The muscle development of early juvenile worms began with dorso-lateral trunk muscles, lateral trunk bands, and sphincters around the gill pores and anus. Adult worms are characterized by a stomochord that bifurcates anteriorly into paired vermiform processes, gill bars that extend almost the entire dorsal to ventral branchial region resulting in a narrow ventral hypobranchial ridge, and an elaborate epibranchial organ with six zones of discrete cell types. The trunk has up to three rows of liver sacs, and lateral gonads. The acorn worm evo-devo model species Saccoglossus kowalevskii, Ptychodera flava, and Schizocardium californicum are phylogenetically distant with disparate life histories. S. karnakawa from S. californicum are phylogenetically close, and differences between them that become apparent as adult worms include the number of gill pores and hepatic sacs, and elaborations of the heart–kidney–stomochord complex. An important challenge for evolutionary developmental biology is to form links from phylogenetically distant and large-scale differences to phylogenetically close and small-scale differences. This description of the embryology, development, and adult morphology of S. karankawa permits investigations into how acorn worm development evolves at fine scales.

This study investigated the fatty acid (FA) composition of total lipids in Quatuoralisia malakhovi Ezhova et Lukinykh, 2022 (Hemichordata, Enteropneusta), a new species of deep-sea acorn worm that was collected on the slope of the Piip Volcano in the Bering Sea. The data we obtained indicate that the main components of lipids in Q. malakhovi are fatty acids of bacterial and diatom origin. The food source of the studied species is detritus containing large amounts of not only bacteria, but also diatoms. These results could be used in trophic studies of communities that include Enteropneusta. [ABSTRACT FROM AUTHOR]

Schizocardium karankawa sp. nov. has been collected from subtidal muds of the Laguna Madre, Texas, and the Mississippi coast, Gulf of Mexico. The Texas population is reproductive from early February to mid-April. Gametes are liberated by a small incision in a gonad. Oocyte germinal vesicle breakdown is increased in the presence of sperm, and the highest fertilization success was in the artificial seawater Jamarin U. Manually dechorionated embryos develop normally. Development was asynchronous via a tornaria larva, metamorphosis and maintained to the juvenile worm 6 gill-pore stage. Phalloidin-labeled late-stage tornaria revealed retractor muscles that connect the pericardial sac with the apical tuft anteriorly, the oesophagus ventrally, and muscle cells of the early mesocoels. The muscle development of early juvenile worms began with dorso-lateral trunk muscles, lateral trunk bands, and sphincters around the gill pores and anus. Adult worms are characterized by a stomochord that bifurcates anteriorly into paired vermiform processes, gill bars that extend almost the entire dorsal to ventral branchial region resulting in a narrow ventral hypobranchial ridge, and an elaborate epibranchial organ with six zones of discrete cell types. The trunk has up to three rows of liver sacs, and lateral gonads. The acorn worm evo-devo model species Saccoglossus kowalevskii, Ptychodera flava, and Schizocardium californicum are phylogenetically distant with disparate life histories. S. karnakawa from S. californicum are phylogenetically close, and differences between them that become apparent as adult worms include the number of gill pores and hepatic sacs, and elaborations of the heart–kidney–stomochord complex. An important challenge for evolutionary developmental biology is to form links from phylogenetically distant and large-scale differences to phylogenetically close and small-scale differences. This description of the embryology, development, and adult morphology of S. karankawa permits investigations into how acorn worm development evolves at fine scales. [ABSTRACT FROM AUTHOR]

Specimens of a new species of torquaratorid acorn worm (Hemichordata, Enteropneusta) were video recorded and subsequently collected at abyssal depths in the eastern North Pacific at sites ranging from Oregon to northern Mexico. These worms are described here as Yoda demiankoopi n. sp. by molecular and morphological methods. The new species differs from its only described congener, Yoda purpurata, in three ways. First, the lips are extremely wide and indented by a deep ciliary groove for ingesting substrate and conveying it to the mouth. Second, a connective tissue bulge of unknown significance runs mid‐dorsally along the hepatic and posthepatic regions of the intestine. Third, the posthepatic intestine is strikingly sinuous and packed with gut contents presumably undergoing digestion for extended periods between infrequent defecations. Yoda demiankoopi n. sp. is hermaphroditic, a character so far known only for the genus Yoda in the entire class Enteropneusta. The gonads of each adult worm comprise hundreds of ovaries (each containing a single oocyte) and hundreds of testes located just beneath the dorsal epidermis of the anterior trunk and associated genital wings. In any given animal, at any given time, gametes of only one sex or the other become fully mature. Thus, the worm is a sequential hermaphrodite, alternately spawning purely as a female or purely as a male. [ABSTRACT FROM AUTHOR]

Here, we describe the shape and mineral composition of ossicles from eight acorn worm species, bringing the total known biomineralizing enteropneusts to 10 and confirming that ossicles are widespread in Enteropneusta. Three general forms were identified including a globular form that occurs in all three major enteropneust families. The biomineral compositions included all three polymorphs of calcium carbonate; calcite, aragonite and vaterite, and low to high magnesium concentrations. Calcite was the most common and characteristic of echinoderm ossicles. Based on these findings we hypothesize that an enteropneust-like ancestor to the Ambulacraria had ectodermal ossicles, formed in an extracellular occluded space bordered by a sheath of sclerocyte cells. The ossicles were microscopic, monotypic globular shaped, calcite ossicles with low to high Mg content and MSP130 proteins. The ossicles lacked intercalation with other ossicles. The function of acorn worm ossicles is unknown, but the position of ossicles in the trunk epithelia and near to the surface suggests predator deterrence, to provide grip on the walls of a burrow or tube, as storage of metabolic waste, or to regulate blood pH, rather than as an endoskeleton function seen in fossil and crown group Echinodermata.

Deep-sea hemichordates Torquaratoridae gen. sp. reach high abundance up to 12 spec. m–2 at the depths of 1830–2130 m on the slope of the Volcanologists Massif in the south-western part of the Bering Sea, dominating in the benthic community at these depths. Their abundance exceeds by two orders the values recorded earlier. In order to clarify this phenomenon, we examined the gut contents of Torquaratoridae gen. sp. The detritus particles and frustules of planktonic diatoms Thalassiosira, Coscinodiscus, Actinocyclus, Chaetoceros, Neodenticula, and Grammatophora were the most common in the gut, as well as the remains of skeletons of benthic invertebrates with little admixture of mineral particles. According to obtained data, Torquaratoridae gen. sp. are mobile deposit feeders with high selectivity to fresh phytodetritus, able to compete with holothurians occupying similar trophic niche. Unusually high abundance of acorn worms is apparently related to high organic matter flux to the seafloor as a result of spring phytoplankton bloom in the surface water layer of the Bering Sea. [ABSTRACT FROM AUTHOR]

Abstract Background Enteropneusts are benthic marine invertebrates that belong to the deuterostome phylum Hemichordata. The two main clades of enteropneusts are defined by differences in early life history strategies. In the Spengelidae and Ptychoderidae, development is indirect via a planktotrophic tornaria larva. In contrast, development in the Harrimanidae is direct without an intervening larval life history stage. Most molecular studies in the development and evolution of the enteropneust adult body plan have been carried out in the harrimanid Saccoglossus kowalevskii. In order to compare these two developmental strategies, we have selected the spengelid enteropneust Schizocardium californicum as a suitable indirect developing species for molecular developmental studies. Here we describe the methods for adult collecting, spawning and larval rearing in Schizocardium californicum, and describe embryogenesis, larval development, and metamorphosis, using light microscopy, immunocytochemistry and confocal microscopy. Results Adult reproductive individuals can be collected intertidally and almost year-round. Spawning can be triggered by heat shock and large numbers of larvae can be reared through metamorphosis under laboratory conditions. Gastrulation begins at 17 h post-fertilization (hpf) and embryos hatch at 26 hpf as ciliated gastrulae. At 3 days post-fertilization (dpf), the tornaria has a circumoral ciliary band, mouth, tripartite digestive tract, protocoel, larval muscles and a simple serotonergic nervous system. The telotroch develops at 5 dpf. In the course of 60 days, the serotonergic nervous system becomes more elaborate, the posterior coeloms develop, and the length of the circumoral ciliary band increases. At the end of the larval stage, larval muscles disappear, gill slits form, and adult muscles develop. Metamorphosis occurs spontaneously when the larva reaches its maximal size (ca. 3 mm), and involves loss and reorganization of larval structures (muscles, nervous system, digestive tract), as well as development of adult structures (adult muscles, tripartite body organization). Conclusions This study will enable future research in S. californicum to address long standing questions related to the evolution of axial patterning mechanisms, germ layer induction, neurogenesis and neural patterning, the mechanisms of metamorphosis, the relationships between larval and adult body plans, and the evolution of metazoan larval forms.

The origin of the notochord is a central issue in chordate evolution. This study examined the development of the acorn worm pygochord, a putative homologue of the notochord. Because the pygochord differentiates only after metamorphosis, the developmental was followed process by inducing regeneration after artificial amputation in Ptychodera flava. It was found that although the regeneration of the posterior part of the body did not proceed via formation of an obvious regeneration bud, pygochord regeneration was observed within a few weeks, possibly via trans‐differentiation of endoderm cells. The expression of the fibrillary collagen gene (Fcol) and elav in the pygochord during regeneration was detected. This indicates that pygochord cells are not part of gut epithelial cells, but that they differentiated as a distinct cell type. Our gene expression analyses do not provide supporting evidence for the homology between the pygochord and notochord, but rather favored the convergent evolution between them. This study examined the regeneration of the acorn worm pygochord, a putative origin of the notochord. We detected the expression of the fibrillary collagen gene and elav in the pygochord during regeneration. [ABSTRACT FROM AUTHOR]

Abstract Hemichordates are a phylum of marine invertebrate deuterostomes that are closely related to chordates, and represent one of the most promising models to provide insights into early deuterostome evolution. The genome of the hemichordate, Saccoglossus kowalevskii, reveals an extensive set of non-coding elements conserved across all three deuterostome phyla. Functional characterization and cross-phyla comparisons of these putative regulatory elements will enable a better understanding of enhancer evolution, and subsequently how changes in gene regulation give rise to morphological innovation. Here, we describe an efficient method of transgenesis for the characterization of non-coding elements in S. kowalevskii. We first test the capacity of an I-SceI transgenesis system to drive ubiquitous or regionalized gene expression, and to label specific cell types. Finally, we identified a minimal promoter that can be used to test the capacity of putative enhancers in S. kowalevskii. This work demonstrates that this I-SceI transgenesis technique, when coupled with an understanding of chromatin accessibility, can be a powerful tool for studying how evolutionary changes in gene regulatory mechanisms contributed to the diversification of body plans in deuterostomes. Highlights • We describe an efficient transgenesis technique in S. kowalevskii - the first transgenic approach in a hemichordate species. • I-SceI meganuclease-mediated transgenesis can drive ubiquitous or regionalized gene expression in live hemichordate embryos. • With this transgenesis system it is possible to label individual cell types, including neurons. • We demonstrate a minimal promoter system that can be used to test putative enhancers in S. kowalevskii. [ABSTRACT FROM AUTHOR]

The enteropneust family Torquaratoridae, discovered in 2005, has the fewest species of the four living families. It is composed of seven species that live on the cold, deep-sea floor. Torquarator bullocki Holland, Clague, Gordon, Gebruk, Pawson and Vecchione, 2005 was the first species described and collected from the Northeastern Pacific. Two new species of Torquaratoridae were collected from the Eastern Pacific and described as Tergivelum baldwinae Holland, Jones, Ellena, Ruhl and Smith, 2009 and Allapasus aurantiacus Holland, Kuhnz and Osborn, 2012. A further three species have been collected from the North Atlantic: Yoda purpurata Priede, Osborn, Gebruk, Jones, Shale, Rogacheva and Holland, 2012, Allapasus isidis Priede, Osborn, Gebruk, Jones, Shale, Rogacheva and Holland, 2012, and Tergivelum cinnabarinum Priede, Osborn, Gebruk, Jones, Shale, Rogacheva and Holland, 2012. The latest Torquaratoridae species was collected from the Russian Arctic in 2013. We add two new species to the Torquaratoridae from Baffin Bay and Viscount Melville Sound, in the eastern Arctic of Canada. Terminstomo arcticus gen. nov. and sp. nov. was collected at a depth of 505 m and is characterized by lacking a heart and a stomochord that extends from the posterior end of the proboscis through the entire length of the collar. Allapasus fuscus sp. nov. was collected from a depth of 444 m and is characterized by a typhlosole process along the dorsal midline of the collar buccal cavity. [ABSTRACT FROM AUTHOR]

Hemichordates are marine invertebrates that are closely related to chordates, but while their body plans are comparable to those of chordates, they possess a remarkable capacity for regeneration, even as adults. A small fragment is sufficient to form a complete individual. Unlike echinoderms, their larvae transform directly into adults; therefore, hemichordate systems offer clear morphological and molecular parallels between regeneration and development. Morphological events in regeneration are generally similar to organogenesis in juveniles. Nonetheless, comparative analysis of gene expression in these two morphological phenomena suggests that hemichordate regeneration is regulated by regeneration‐specific mechanisms, as well as by developmental mechanisms. Dependency upon resident pluripotent/multipotent stem cells is a significant difference in metazoan regeneration, and such stem cells are essential for regeneration in many lineages. Based on the present gene expression study, regeneration in acorn worms is more closely related to that in vertebrates, because it employs endogenous stem cell‐independent transdifferentiation. [ABSTRACT FROM AUTHOR]

Phylum Hemichordata, composed of worm-like Enteropneusta and colonial Pterobranchia, has been reported to only contain about 100 species. However, recent studies of hemichordate phylogeny and taxonomy suggest the species number has been largely underestimated. One issue is that species must be described by experts, and historically few taxonomists have studied this group of marine invertebrates. Despite this previous lack of coverage, interest in hemichordates has piqued in the past couple of decades, as they are critical to understanding the evolution of chordates–as acorn worms likely resemble the deuterostome ancestor more closely than any other extant animal. This review provides an overview of our current knowledge of hemichordates, focusing specifically on their global biodiversity, geographic distribution, and taxonomy. Using information available in the World Register of Marine Species and published literature, we assembled a list of 130 described, extant species. The majority (83%) of these species are enteropneusts, and more taxonomic descriptions are forthcoming. Ptychoderidae contained the greatest number of species (41 species), closely followed by Harrimaniidae (40 species), of the recognized hemichordate families. Hemichordates are found throughout the world’s oceans, with the highest reported numbers by regions with marine labs and diligent taxonomic efforts (e.g. North Pacific and North Atlantic). Pterobranchs are abundant in Antarctica, but have also been found at lower latitudes. We consider this a baseline report and expect new species of Hemichordata will continue to be discovered and described as new marine habitats are characterized and explored. [ABSTRACT FROM AUTHOR]

Reports on the abundances and on metal concentrations in intertidal estuarine invertebrates from the Eastern Tropical Pacific are rare. Thus, the objectives of this report are to make accessible data on the abundances (1984-1987, 49 dates; 2013, 12 dates) of sipunculans, brachiopods and hemichordates from a sand-mud flat; and on trace metals (1996, 2000) and abundances (2015, 3 dates) of sipunculans and brachiopods at a sand flat in the Gulf of Nicoya estuary (10° N-85° W). Cores (17.7 cm²) were collected at the sand-mud flat, and quadrats (0.2 m2) at the sand flat. The flats contrasted in their sand (65% vs 90%) and silt+clay (31.5% vs 5.6%) contents. At the sand-mud flat (1984-87: 1.83 m²) the sipunculans were represented by 13 individuals, the brachiopods by 129 and the acorn worms by 185, with estimated maximum densities of: 5.7, 29, and 40 ind./m², respectively. Trace metal (Fe, Mn, Ni, Cr, Cd, Zn, and Pb) analysis (Atomic Absorption Spectrometry) were conducted in specimens of Sipunculus nudus (Sipuncula) and Glottidia audebarti (Brachiopoda). Maximum mean concentrations in S. nudus were: For non-depurated worms, Fe (16.0 mg/g dw) > Mn (165 μg/g dw) > Zn (81 μg/g dw) > Cu (26 μg/g dw) > Cr (11 μg/g dw) > Ni (10.4 μg/g dw) > Pb (9.3 μg/g dw) > Cd (1.2 μg/g dw). For 72 hour depurated worms: Fe (5.0 mg/g dw) > Mn (61 μg/g dw) > Zn (39 μg/g dw) > Cu (24 μg/g dw) > Ni (8.4 μg/g dw) > Pb (2.7 μg/g dw) > Cd (0.62 μg/g dw). For G. audebarti: Fe (1.6 mg/g dw-soft parts) > Zn (123.5 μg/g dw-soft parts) > Cu (31.4 μg/g dw-pedicles) > Pb (21.0 μg/g dw-shells) > Cd (5.2 μg/g dw-soft parts) > Cr (4.7 μg/g dw-shells). For sediments; Fe (46 mg/g dw) > Mn (41.3 μg/g dw) > Zn (63 μg/g dw) > Cu (36.2 μg/g dw) > Cr (31.5 μg/g dw) > Pb (21.1 μg/g dw) > Ni (16.1 μg/g dw) > Cd (1.1 μg/g dw). These concentrations were expected for a nonindustrialized estuary. At the sand flat (Area sampled: 10.6 m²) 76 individuals of G. audebarti, 112 of G. albida, and 366 of S. nudus were collected in 2015, with estimated maximum densities of: 7.1, 10.5, and 31 ind./m2, respectively. Densities of G. audebarti and G. albida were relatively low, while those of S. nudus were relatively high when compared with other reports. The shell lenght of G. audebarti ranged from 9.0 mm to 38.0 mm and from 6.0 mm to 29.0 mm for G. albida. These ranges were within those found for these lingulides elsewhere. The mean length of S. nudus was 41 mm and the maximum weight was 1.6 g, which are small. No brachiopods were found at the sand-mud flat in 2013, nor enteropneusts at the sand flat in 2015. G. audebarti had a relatively stable presence, while G. albida almost vanished from the samples at the end of 2015. The spatial distributions of the three invertebrates were found aggregated at both intertidal flats. Strong ENSO warming events during 1983 and 2015, and red tides in 1985 may have influenced the abundances. Rev. Biol. Trop. 64 (3): 1311-1331. Epub 2016 September 01. [ABSTRACT FROM AUTHOR]

Hemichordates are marine animals with two different lifestyles. The solitary, free-living enteropneusts or acorn worms resemble polychaetes or earthworms, while the tiny, colonial, sessile pterobranchs are similar to bryozoans and phoronids. Hemichordates, together with echinoderms, comprise the clade Ambulacraria and are a sister group to the Chordata. As adults, they exhibit cardinal chordate characters, such as gill slits. Their embryogenesis and dipleurula-type (tornaria) larvae are very similar to those of echinoderms. Recent advances in comparative genomics and molecular developmental biology of hemichordates, especially the vermiform enteropneusts, have shed light on deuterostome ancestors. This paper briefly reviews the numerous recent studies on the Phylum Hemichordata. [ABSTRACT FROM AUTHOR]

Background: The combination of a meager fossil record of vermiform enteropneusts and their disparity with the tubicolous pterobranchs renders early hemichordate evolution conjectural. The middle Cambrian Oesia disjuncta from the Burgess Shale has been compared to annelids, tunicates and chaetognaths, but on the basis of abundant new material is now identified as a primitive hemichordate. Results: Notable features include a facultative tubicolous habit, a posterior grasping structure and an extensive pharynx. These characters, along with the spirally arranged openings in the associated organic tube (previously assigned to the green alga Margaretia), confirm Oesia as a tiered suspension feeder. Conclusions: Increasing predation pressure was probably one of the main causes of a transition to the infauna. In crown group enteropneusts this was accompanied by a loss of the tube and reduction in gill bars, with a corresponding shift to deposit feeding. The posterior grasping structure may represent an ancestral precursor to the pterobranch stolon, so facilitating their colonial lifestyle. The focus on suspension feeding as a primary mode of life amongst the basal hemichordates adds further evidence to the hypothesis that suspension feeding is the ancestral state for the major clade Deuterostomia. [ABSTRACT FROM AUTHOR]

The limited fossil record of enteropneust hemichordates (acorn worms) and the few external features that distinguish the four families have provided a challenge to our understanding of the evolution of the group and their various feeding adaptations. The middle Pennsylvanian Saccoglossus testa sp. nov. from the Mazon Creek, Westfalian D Carbonate Formation, Francis Creek Shale of northern Illinois provides evidence for the exploitation of surface sediments. Saccoglossus testa has a long proboscis characteristic of the extant genus Saccoglossus, a specialist in surface deposit feeding. The collar is as long as it is wide. The anterior trunk lacks a distinctively wide branchial region. These three features distinguish it from its sympatric enteropneust species Mazoglossus ramsdelli Bardack that has a proboscis characteristic of an infaunal deposit feeder. It is the seventh known species of fossil enteropneust, including a resting trace of a Lower Triassic fossil that has collar lips that characterize the extant deep-sea family Torquaratoridae, and which represents a second parallel evolution of surface deposit feeding. An analysis of the seven fossils shows that the earliest Enteropneusta had a relatively simple harrimaniid-like body plan, and that the spengelid, the torquaratorid and lastly the most complex ptychoderid body plan appeared in that chronological order. [ABSTRACT FROM AUTHOR]

Older evolutionary scenarios for the origin of vertebrates often gave nervous systems top billing in accordance with the notion that a big-brained Homo sapiens crowned a tree of life shaped mainly by progressive evolution. Now, however, tree thinking positions all extant organisms equidistant from the tree's root, and molecular phylogenies indicate that regressive evolution is more common than previously suspected. Even so, contemporary theories of vertebrate origin still focus on the nervous system because of its functional importance, its richness in characters for comparative biology, and its central position in the two currently prominent scenarios for the invertebrate-tovertebrate transition, which grew out of the markedly neurocentric annelid and enteropneust theories of the nineteenth century. Both these scenarios compare phyla with diverse overall body plans. This diversity, exacerbated by the scarcity of relevant fossil data, makes it challenging to establish plausible homologies between component parts (e.g. nervous system regions). In addition, our current understanding of the relation between genotype and phenotype is too preliminary to permit us to convert gene network data into structural features in any simpleway. These issues are discussed here with special reference to the evolution of nervous systems during proposed transitions from invertebrates to vertebrates. [ABSTRACT FROM AUTHOR]

ABSTRACT The indirect-developing enteropneust acorn worm Ptychodera flava has been used as a hemichordate model system for studying the developmental evolution of deuterostome body plans and the origins of chordate characteristics. However, research progress has been hindered by the limited accessibility of its embryonic materials and metamorphosing larvae. In this study, we identified an abundant population of P. flava in Penghu, Taiwan, and examined the feasibility of using this animal for developmental studies. Through histological examination, we established that the reproductive season of this population is between September and December, with a peak breeding period in October and November. In addition, we have developed new procedures that can induce P. flava spawning at any time of the day during the breeding season, with a higher successful rate than that achieved using a previously published method. Moreover, the culturing system we developed enables rearing of P. flava larvae through various planktonic stages and eventual metamorphosis into benthic juveniles, all under laboratory conditions. We anticipate that the animal resources and new technical procedures reported here will further facilitate the use of P. flava as a model organism for evolutionary and developmental biology research. J. Exp. Zool. (Mol. Dev. Evol.) 326B:47-60, 2016. © 2015 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

Acorn worms, also known as enteropneust (literally, 'gut-breathing') hemichordates, are marine invertebrates that share features with echinoderms and chordates. Together, these three phyla comprise the deuterostomes. Here we report the draft genome sequences of two acorn worms, Saccoglossus kowalevskii and Ptychodera flava. By comparing them with diverse bilaterian genomes, we identify shared traits that were probably inherited from the last common deuterostome ancestor, and then explore evolutionary trajectories leading from this ancestor to hemichordates, echinoderms and chordates. The hemichordate genomes exhibit extensive conserved synteny with amphioxus and other bilaterians, and deeply conserved non-coding sequences that are candidates for conserved gene-regulatory elements. Notably, hemichordates possess a deuterostome-specific genomic cluster of four ordered transcription factor genes, the expression of which is associated with the development of pharyngeal 'gill' slits, the foremost morphological innovation of early deuterostomes, and is probably central to their filter-feeding lifestyle. Comparative analysis reveals numerous deuterostome-specific gene novelties, including genes found in deuterostomes and marine microbes, but not other animals. The putative functions of these genes can be linked to physiological, metabolic and developmental specializations of the filter-feeding ancestor. [ABSTRACT FROM AUTHOR]

The transformer ( tra) gene is an intermediate component of the sex determination hierarchy in many insect species. The homolog of tra is also found in two branchiopod crustacean species but is not known outside arthropods. We have isolated a tra homolog in the acorn worm, Saccoglossus kowalevskii, which is a hemichordate belonging to the deuterostome superphylum. The full-length complementary DNA (cDNA) of the S. kowalevskii tra homolog ( Sktra) has a 3786-bp open reading frame that encodes a 1261-amino acid sequence including a TRA-CAM domain and an arginine/serine (RS)-rich domain, both of which are characteristic of TRA orthologs. Reverse transcription PCR (RT-PCR) analyses demonstrated that Sktra showed no differences in expression patterns between testes and ovaries, but its expression level was approximately 7.5-fold higher in the testes than in the ovaries. TRA, together with the protein product of the transformer-2 ( tra-2) gene, assembles on doublesex ( dsx) pre-messenger RNA (mRNA) via the cis-regulatory element, enhancing female-specific splicing of dsx in Drosophila. To understand functional conservation of the SkTRA protein as a dsx-splicing activator, we investigated whether SkTRA is capable of inducing female-specific splicing of the Drosophila dsx. Ectopic expression of Sktra cDNA in insect cultured cells did not induce the female-specific splicing of dsx. On the other hand, forced expression of Sktra-2 (a tra-2 homolog of S. kowalevskii) was able to induce the female-specific dsx splicing. These results demonstrate that the function as a dsx-splicing activator is not conserved in SkTRA even though SkTRA-2 is capable of functionally replacing the Drosophila TRA-2. We have also found a tra homolog in an echinoderm genome. This study provides the first evidence that that tra is conserved not only in arthropods but also in basal species of deuterostoms. [ABSTRACT FROM AUTHOR]

Concerning the evolution of deuterostomes, enteropneusts (acorn worms) occupy a pivotal role as they share some characteristics with chordates (e.g., tunicates and vertebrates) but are also closely related to echinoderms (e.g., sea urchin). The nervous system in particular can be a highly informative organ system for evolutionary inferences, and advances in fluorescent microscopy have revealed overwhelming data sets on neurogenesis in various clades. However, immunocytochemical descriptions of neurogenesis of juvenile enteropneusts are particularly scarce, impeding the reconstruction of nervous system evolution in this group. We followed morphogenesis of the nervous system in two enteropneust species, one with direct ( Saccoglossus kowalevskii) and the other with indirect development ( Balanoglossus misakiensis), using an antibody against serotonin and electron microscopy. We found that all serotonin-like immunoreactive (LIR) neurons in both species are bipolar ciliary neurons that are intercalated between other epidermal cells. Unlike the tornaria larva of B. misakiensis, the embryonic nervous system of S. kowalevskii lacks serotonin-LIR neurons in the apical region as well as an opisthotroch neurite ring. Comparative analysis of both species shows that the projections of the serotonin-LIR somata initially form a basiepidermal plexus throughout the body that disappears within the trunk region soon after settlement before the concentrated dorsal and ventral neurite bundles emerge. Our data reveal a highly conserved mode of neurogenesis in enteropneusts that is independent of the developing mode and is inferred to be a common feature for Enteropneusta. Moreover, all detected serotonin-LIR neurons are presumably receptor cells, and the absence of serotonin-LIR interneurons from the enteropneust nervous system, which are otherwise common in various bilaterian central nervous systems, is interpreted as a loss that might have occurred already in the last common ancestor of Ambulacraria. [ABSTRACT FROM AUTHOR]

Enteropneusts or acorn worms are marine deuterostomes that have retained many plesiomorphic characters. Thus, enteropneusts are of prime interest in evolutionary comparisons between deuterostomes and protostomes. In the present study, the larval eyes of Glossobalanus marginatus were reconstructed and described based on serial sectioning for transmission electron microscopy. The everse eyes of the late Metschnikoff/early Krohn-stage tornaria larvae of G. marginatus are epidermal structures consisting of two rows of in total 13 shading pigment cells and another two rows of 13 photoreceptor cells. The pigment cells form a shallow cup with a relatively wide opening, making the cup-shaped eye optically unsuitable for picture generation. We demonstrate that the photosensitive cells possess numerous enlarged microvilli and an unmodified apical cilium. Our ultrastructural studies thus corroborate the photoreceptor cells in the eye of G. marginatus to be of a clearly rhabdomeric type. Preliminary immunohistochemical experiments support those findings by demonstrating immunopositive reaction of the tornarian eye photoreceptors with an antibody designed against rhabdomeric sea urchin photopigment (Sp-Opsin4). Observations of living animals indicate that Late Metschnikoff/early Krohn-stage tornaria larvae are negatively phototactic, probably concordant with imminent metamorphosis. [ABSTRACT FROM AUTHOR]

Over the past 200 years, almost every invertebrate phylum has been proposed as a starting point for evolving vertebrates. Most of these scenarios are outdated, but several are still seriously considered. The short-range transition from ancestral invertebrate chordates (similar to amphioxus and tunicates) to vertebrates is well accepted. However, longer-range transitions leading up to the invertebrate chordates themselves are more controversial. Opinion is divided between the annelid and the enteropneust scenarios, predicting, respectively, a complex or a simple ancestor for bilaterian animals. Deciding between these ideas will be facilitated by further comparative studies of multicellular animals, including enigmatic taxa such as xenacoelomorphs. [ABSTRACT FROM AUTHOR]

Abstract: The Hemichordata are generally interpreted as early deuterostomes, closely related to the chordates, a notion important for modern analyses of the origin of the deuterostomes. Because their fossil record is quite scanty, modern phylogenetic interpretations largely rely on the analysis of DNA of the available extant taxa. The tripartite body plan of the group of worm-like hemichordates, the Enteropneusta, may be traced back in deep time to a few poorly known Middle Cambrian (Series 3, Stage 5) taxa from the Burgess Shale biota. The derived small, colonial or pseudocolonial Pterobranchia (Cephalodiscida and Graptolithina) have a more complete fossil record due to their preservable housing construction, the tubarium. The relationships of fossil taxa, putatively identified as early deuterostomes and possible hemichordates or even as pterobranchs of Lower to Middle Cambrian age (e.g. Galeaplumosus, Herpetogaster), cannot be substantiated. The Pterobranchia and their housing construction are first seen in the Middle Cambrian Series 3, Stage 5 but a clonal, colonial organization of the tubaria can only be recognized in the basal Drumian. The fossil enteropneust Mazoglossus ramsdelliBardack, 1997 from the Carboniferous Mazon Creek Biota is re-described, its lectotype designated and illustrated for the first time. [Copyright &y& Elsevier]

Symbiotic copepods compose one-third of the known copepod species and are associated with a wide range of animal groups. Two parasitic copepods endoparasitic in acorn worms (Hemichordata), Ive balanoglossi and Ubius hilli, collected in the Mediterranean Sea and Australian waters, respectively, were described a century ago. Here we report a new parasitic copepod species, Ive ptychoderae sp. nov., found in Ptychodera flava, a widespread acorn worm in the Indo-Pacific Ocean and an emerging organism for developmental and evolutionary studies. The female of I. ptychoderae is characterized by having a reduced maxilliped and five pairs of annular swellings along the body that are morphologically similar but distinguishable from those in the two previously described parasitic copepods in acorn worms. Phylogenetic analysis based on the 18S rDNA sequence shows that I. ptychoderae may belong to Poecilostomatoida but represent a new family, which we name Iveidae fam. nov. Ive ptychoderae is commonly found in the acorn worm population with an average prevalence of 42% during the collecting period. The infection of the parasite induces the formation of cysts and causes localized lesions of the host tissues, suggesting that it may have negative effects on its host. Interestingly, most cysts contain a single female with one or multiple male copepods, suggesting that their sex determination may be controlled by environmental conditions. The relationships between the parasitic copepods and acorn worms thus provide a platform for understanding physiological and ecological influences and coevolution between parasites and hosts. [ABSTRACT FROM AUTHOR]

The ecology, distribution and mode of life of three species of surface-dwelling enteropneusts is described, based on ROV observations and samples on the flanks of the Northern Mid-Atlantic Ridge (MAR) at comparative stations north and south of the Sub-Polar Front. Tergivelum cinnabarinum was most abundant in the north (mean=4.56 ind. 1000m−2±3.50 s.d.) and occurred at low densities in the south (mean=1.19±1.68 s.d.). Yoda purpurata was dominant in the south (mean=17.00 ind. 1000m−2±12.32 s.d.) but only one individual was found in the north. The within-station distribution of all enteropneust species encountered was generally random. T. cinnabarinum was larger (mean total length 142mm) than Y. purpurata (mean total length 70mm). Size distributions suggested smaller individuals of both species on the western side of the MAR. Size and density of enteropneusts were generally higher in areas with higher carbon flux to the seafloor. A single individual of Allapasus isidis was observed drifting and settling to the seafloor at the SW site. Traces on the seafloor made by T. cinnabarinum covered a much higher percentage of the total seabed area surveyed (mean=0.323%±0.155 s.d.) than those of Y. purpurata (mean=0.034%±0.037 s.d.). Stable isotope values for T. cinnabarinum suggested that it was a typical surficial deposit feeder. Enteropneusts appear to be abundant and an important bioturbator on the sedimented seafloor of the MAR at around 2500m depth. [ABSTRACT FROM AUTHOR]

A 2009 oceanographic expedition of the Russian Academy of Sciences collected the anterior region of a single acorn worm (phylum Hemichordata, class Enteropneusta) by trawling at a depth of 5560 m in the Romanche Trench (equatorial Atlantic). The specimen was a ripe female with numerous, relatively small oocytes in each ovary. Phylogenetic analysis of rDNA sequences robustly placed the worm in the family Spengelidae. In addition, morphological features of the proboscis, collar, and anterior trunk region indicated that the worm was Glandiceps abyssicola, a species previously represented solely by the holotype, which had been dredged from the equatorial Atlantic in 1873 by the HMS ‘Challenger’ and subsequently sent to Germany for description by Spengel (1893). The holotype was presumably destroyed by World War II bombing; therefore, we here designate the Romanche Trench specimen as the neotype of G. abyssicola and supply an augmented species diagnosis. [ABSTRACT FROM PUBLISHER]

Here, we describe the shape and mineral composition of ossicles from eight acorn worm species, bringing the total known biomineralizing enteropneusts to 10 and confirming that ossicles are widespread in Enteropneusta. Three general forms were identified including a globular form that occurs in all three major enteropneust families. The biomineral compositions included all three polymorphs of calcium carbonate; calcite, aragonite and vaterite, and low to high magnesium concentrations. Calcite was the most common and characteristic of echinoderm ossicles. Based on these findings we hypothesize that an enteropneust-like ancestor to the Ambulacraria had ectodermal ossicles, formed in an extracellular occluded space bordered by a sheath of sclerocyte cells. The ossicles were microscopic, monotypic globular shaped, calcite ossicles with low to high Mg content and MSP130 proteins. The ossicles lacked intercalation with other ossicles. The function of acorn worm ossicles is unknown, but the position of ossicles in the trunk epithelia and near to the surface suggests predator deterrence, to provide grip on the walls of a burrow or tube, as storage of metabolic waste, or to regulate blood pH, rather than as an endoskeleton function seen in fossil and crown group Echinodermata., (© 2022 The Authors.)

Introduction: Traditionally, the origin of the third germ layer and its special formation of coelomic cavities by enterocoely is regarded to be an informative character in phylogenetic analyses. In early deuterostomes such as sea urchins, the mesoderm forms through a single evagination pinching off from the apical end of the archenteron which then gives off mesocoela and metacoela on each side. This echinoid-type coelom formation has conventionally been assumed to be ancestral for Deuterostomia. However, recent phylogenetic analyses show that Echinodermata hold a more derived position within Deuterostomia. In this regard a subgroup of Hemichordata, namely enteropneusts, seem to host promising candidates, because they are supposed to have retained many ancestral deuterostome features on the one hand, and furthermore share some characteristics with chordates on the other hand. In enteropneusts a wide range of different modes of coelom formation has been reported and in many cases authors of the original observations carefully detailed the limitations of their descriptions, while these doubts disappeared in subsequent reviews. In the present study, we investigated the development of all tissues in an enteropneust, Saccoglossus kowalevskii by using modern morphological techniques such as complete serial sectioning for LM and TEM, and 3D-reconstructions, in order to contribute new data to the elucidation of deuterostome evolution. Results: Our data show that in the enteropneust S. kowalevskii all main coelomic cavities (single protocoel, paired mesocoela and metacoela) derive from the endoderm via enterocoely as separate evaginations, in contrast to the aforementioned echinoid-type. The anlagen of the first pair of gill slits emerge at the late kink stage (~96 h pf). From that time onwards, we documented a temporal left-first development of the gill slits and skeletal gill rods in S. kowalevskii until the 2 gill slit juvenile stage. Conclusions: The condition of coelom formation from separate evaginations is recapitulated in the larva of amphioxus and can be observed in crinoid echinoderms in a similar way. Therefore, coelom formation from separated pouches, rather than from a single apical pouch with eventual subdivision is suggested as the ancestral type of coelom formation for Deuterostomia. Left-right asymmetries are also present in echinoderms (rudiment formation), cephalochordates (larval development), tunicates (gut coiling) and vertebrates (visceral organs), and it is known from other studies applying molecular genetic analyses that genes such as nodal, lefty and pitx are involved during development. We discuss our findings in S. kowalevskii in the light of morphological as well as molecular genetic data. [ABSTRACT FROM AUTHOR]

A single specimen of a previously undescribed acorn worm in the family Torquaratoridae was trawled from a bottom depth of about 350 m in the Kara Sea (Russian Arctic). The new species is the shallowest of the exclusively deep-sea torquaratorids found to date, possibly an example of high-latitude emergence. On the basis of ribosomal DNA sequences and morphology, the worm is described here as the holotype of Coleodesmium karaensis n. gen., n. sp. It is most similar in overall body shape to the previously described enteropneust genus Allapasus, but is uniquely characterized by a tubular component of the proboscis skeleton ensheathing the collar nerve cord. Additionally, within the proboscis, the sparseness of the musculature of C. karaensis clearly distinguishes it from the much more muscular members of Allapasus. The holotype is a female bearing about a dozen embryos on the surface of her pharyngeal region, each recessed within a shallow depression in the dorsal epidermis. The embryos, ranging from late gastrula to an early stage of coelom formation, are a little more than 1 mm in diameter and surrounded by a thin membrane. Each embryo comprises an external ectoderm of monociliated cells (not arranged in obvious ciliated bands) and an internal endo-mesoderm; the blastopore is closed. In the most advanced embryos, the anterior coelom is starting to constrict off from the archenteron. Coleodesmium karaensis is the first enteropneust (and indeed the first hemichordate) found brooding embryos on the surface of the mother's body. [ABSTRACT FROM AUTHOR]

Understanding the evolutionary history of deuterostomes requires elucidating the phylogenetic interrelationships amongst the constituent taxa. Although the monophyly and interrelationships among the three principal groups-the chordates, the echinoderms, and the hemichordates-are well established, as are the internal relationships among the echinoderm and chordate taxa, the interrelationships among the principal groups of hemichordates-the harrimaniid enteropneusts, the ptychoderid enteropneusts, and the pterobranchs--remain unresolved. Depending on the study some find enteropneusts paraphyletic with pterobranchs (e.g., Cephalodiscus) more closely related to the harrimaniid enteropneusts (e.g., Saccoglossus) than either are to the ptychoderid enteropneusts (e.g., Ptychodera), whereas other studies support a monophyletic Enteropneusta. To try and resolve between these two competing hypotheses, we turned to microRNAs, small ~22 nt non-coding RNA genes that have been shown to shed insight into particularly difficult phylogenetic questions. Using deep sequencing we characterized the small RNA repertoires of two hemichordate species, Cephalodiscus hodgsoniand Ptychodera flava, and the crinoid echinoderm Antedon mediterráneo, and combined our results with the described complements of the hemichordate Saccoglossus kowalevskii, the sea urchin Strongylocentrotuspurpuratus, and the starfish Patiria miniata. Our data unambiguously support the monophyly of Enteropneusts as S. kowalevskii shares 12 miRNA sequences with P. flava that are not present in the C. hodgsoni or A. mediterráneo libraries, and have never been reported from another metazoan taxon. Thus, these data resolve the phylogenetic position of pterobranchs, ultimately allowing fora better understanding of body plan evolution throughout the deuterostomes [ABSTRACT FROM AUTHOR]

A new species of the genus Protoglossus is described from the west coast of the Scandinavian Peninsula. It lives buried in clay bottoms below the halocline where the salinity is at least 33-34 psu. Body small, estimated maximal length 1.5 cm. Collar broader than long, with a forward inclination. The thickest part is the collar region where it can be up to 1 mm in diameter. Proboscis colouration light pink to golden yellow; collar white with transversal yellow bands; branchial, hepatic and intestinal regions translucent pale yellow to golden yellow; brown intestine visible through the body wall. Proboscis groove extends through posterior half of proboscis. Nine to 17 pairs of gill openings, the size of the posteriormost successively smaller. It differs from the other European species, Protoglossus koehleri, in colouration, smaller size, fewer gill openings, body shape and proportions. It was sequenced (18S rRNA gene) and clustered within the family Harrimaniidae, with Saxipendium as its closest relative. [ABSTRACT FROM AUTHOR]

Ninety-two individuals of a deep-sea harrimaniid enteropneust were imaged between 1675 m and 3225 m off the California coast. Of these, about three-fourths were positioned with their posterior regions buried in sediment or hidden by rocks, and the rest were completely exposed on the substratum. When visible, the posterior end of each worm was typically associated with a dense tangle of fecal strands. One specimen was captured and is described here as the holotype of Saxipendium implication. In life, it was 22 cm long, and the color of its dome-shaped proboscis, narrow collar, and anterior trunk was medium orange. No wing-like folds of the body wall protruded anywhere along the length of the worm. The proboscis complex included a stomochord and glomeruli, but neither a heart nor a pericardial cavity could be detected. Most of the dorsal collar nerve runs along an open invagination in the dorsal midline of the collar and is only roofed over very briefly at the posterior extremity of the collar. Another unusual feature is the exaggerated posterior extension of the horns of the proboscis skeleton, which projected into the anterior extremity of the trunk. The trunk commenced anteriorly with a pharyngeal/esophageal region that included a tract of ovaries on either side of the dorsal midline. The ripest ovaries contained a single oocyte approximately 700 μm in diameter (presumably this species is gonochoric, although no males have yet been collected). The gill skeleton lacked synapticles. More posteriorly, the trunk housed a long, darkly pigmented hepatic intestine without sacculations and a short, lightly pigmented post-hepatic intestine. The geographic range of S. iniplicatum appears to be restricted to the Davidson, Guide, and Taney Seamounts region in the eastern Pacific offshore of Central California. [ABSTRACT FROM AUTHOR]

Here, we report the discovery and characterization of biominerals in the acorn worms Saccoglossus bromophenolosus and Ptychodera flava galapagos (Phylum: Hemichordata). Using electron microscopy, X-ray microprobe analyses and confocal Raman spectroscopy, we show that hemichordate biominerals are small CaCO3 aragonitic elements restricted to specialized epidermal structures, and in S. bromophenolosus, are apparently secreted by sclerocytes. Investigation of urchin biomineralizing proteins in the translated genome and expressed sequence tag (EST) libraries of Saccoglossus kowalevskii indicates that three members of the urchin MSP-130 family, a carbonic anhydrase and a matrix metaloprotease are present and transcribed during the development of S. kowalevskii. The SM family of proteins is absent from the hemichordate genome. These results increase the number of phyla known to biomineralize and suggest that some of the gene-regulatory ‘toolkit’, if not mineralized tissue themselves, may have been present in the common ancestor to hemichordates and echinoderms. [ABSTRACT FROM AUTHOR]

Enteropneusts (phylum Hemichordata), although studied extensively because of their close relationship to chordates, have long been considered shallow-water, burrowing animals. The present paper more than doubles the number of enteropneust species recorded in the deep sea based on high-resolution imaging and sampling with remotely operated vehicles. We provide direct evidence that some enteropneusts are highly mobile—using changes in posture and currents to drift between feeding sites—and are prominent members of deep, epibenthic communities. In addition, we provide ecological information for each species. We also show that despite their great morphological diversity, most deep-living enteropneusts form a single clade (the rediagnosed family Torquaratoridae) on the basis of rDNA sequences and morphology of the proboscis skeleton and stomochord. The phylogenetic position of the torquaratorids indicates that the group, after evolving from near-shore ancestors, radiated extensively in the deep sea. [ABSTRACT FROM AUTHOR]

Trophic interactions can trigger the development of exaggerated specialized characters and promote morphological diversification. For example, acorn weevils (genus Curculio) present strikingly long rostrums, which are used by females to perforate oviposition holes through the seed coat. Species exhibiting longer rostrums are known to exploit larger acorns, and therefore rostrum length is thought to be subject to selection to match the preferred acorn type. However, rostrum length is strongly correlated with body size, and morphological divergence could result from either selection on rostrum length for optimal food exploitation or from other pressures acting on body size. We collected infested acorns at oak forests where the large Curculio elephas and the small-bodied Curculio glandium co-occur. There were no interspecific differences in adult female body size to rostrum length allometric relationships, and rostrum length is equally correlated with body size in either species. MtDNA-based species identification showed that C. glandium larvae were present within acorns of all sizes, whereas C. elephas larvae were restricted to acorns above a minimum size, irrespective of oak species. Hence, exploitation of large acorns can hardly have triggered rostrum enlargement, as the small sized C. glandium adults (with short rostrums) could perforate and oviposit in both small and large acorns. Rather, increased rostrum length is probably a by-product of the larger body sizes of individuals emerging from bigger acorns, which allow increased larval size and enhance larval survival likelihood. Summarizing, when exaggerated feeding traits co-vary with other body features, interspecific morphological variability may result from contrasting selective pressures acting on these correlated characters. [ABSTRACT FROM AUTHOR]

The article discusses the evolutionary origin of Drosophila Pax transcription factor gene eyegone (eyg) and its functions in development and body plan evolution. It shows that eyg's origin predates metazoan diversification, and says comparative studies of eyg in the sea urchin and acorn worm might disclose eyg's ancient patterning functions. It suggests ignoring eyg's classification as a related gene of Pax6 isoform 5a because their evolutionary histories do not match.