The gills are hypothesized to play a key role in early vertebrate evolution by replacing the skin as the primary site of gas exchange. In this scenario, water flow across the gills for suspension feeding was coopted for gas exchange in stem vertebrates, facilitating the evolution of larger, active fishes. This is supported by a stem-vertebrate origin for structures increasing gill capacity for gas exchange. However, these structures might have enhanced an already dominant capacity at ancestral deuterostome gills. To test this, we characterized gill function in the suspension-feeding hemichordate Protoglossus graveolens. We measured oxygen uptake and ammonia excretion in whole worms and worm halves with or without gills at 10oC and 20oC to stimulate gill recruitment. Gills did not enhance oxygen uptake or ammonia excretion, suggesting they are not a primary site of gas exchange. This provides critical functional support for the long-hypothesized vertebrate origin of gills as the primary gas exchange organ.

The fossil record of medusozoan cnidarians is relatively sparse and, in some cases, contentious. Here, we describe a new genus and species of a well-preserved, soft-bodied, tubicolous polyp, Paleocanna tentaculum n. gen. n. sp., from the Upper Ordovician (Katian) Neuville Formation in Quebec. These fossils, preserved as carbonaceous compressions, were found in association with typical shelly assemblages. Fifteen slabs of shaly limestone containing similar to 135 specimens of Paleocanna tentaculum n. gen. n. sp. were examined. Individual polyps occupied upright tubes, which occur either solitarily or in clusters. Some tubes exhibit a striated periderm near their base. The polyp is elongated, with a rounded aboral end and a consistent ring of tentacles protruding distally from the tube. A phylogenetic analysis of 69 taxa and 236 discrete morphological characters indicated that the species is more closely related to the extant crown group than it is to the other stem-group medusozoans, e.g., conulariids and carinachitids. The uniform orientation of specimens on single slabs suggests rapid burial. Paleocanna tentaculum n. gen. n. sp. represents an exceptionally preserved member of an Ordovician deposit exhibiting Burgess Shale-type soft-tissue preservation.

The fauna of the Fezouata Shale, an Early Ordovician fossil Lagerstätte from Morocco, is transitional between the Cambrian and the Great Ordovician Biodiversification Event (GOBE). We compiled a comprehensive taxa list for the Lower Fezouata Shale and developed its empirical trophic network. We compared it to four modern marine networks and a modeling by the niche model, known for accurately representing modern trophic networks. The Fezouata network, compared with modern ones, had higher proportions of top, herbivore, and basal taxa, indicating a community defined by the coexistance of top predators typical of both the Cambrian and the Ordovician and the dominance of low-trophic-level taxa such as filter-feeders, whose expansion characterized the GOBE. These diversifying taxa were also mostly generalists. The Lower Fezouata trophic network did not significantly differ from its niche model prediction, suggesting that most elements of modern trophic network structure had already appeared by the Early Ordovician.

Benthic filter-feeders form an essential role in marine food chains as they constitute the bridge between the microscopic primary producers and the consumers. Although filter-feeders mainly feed on solid particles, they also capture and ingest oil droplets. Usually, these microdroplets come from the decomposition of animals or algae or from petroleum oils that enter water via spills and leakages. Here, we used videography, TRITC fluorescence microscopy, and fluid mechanics to study the capture mechanisms of canola, fish, and four petroleum motor oil droplets by the filter feeding sabellid and a serpulid polychaetes. Schizobranchia insignis, Eudistylia vancouveri, Myxicola infundibulum and Serpula columbiana actively feed on waste motor oil droplets in seawater. A further experiment found that S. insignis fed on all types of oil droplets, demonstrating no selectivity based on type. The oil droplet capture mechanism of S. insignis were direct interception and sieving, like that of solid particles. The size range of droplets ingested was 10 to 300 µm in diameter, but these ranges differed depending on the density and viscosity of the oils. Higher density and viscous oils were captured at smaller droplet sizes. These results are the first to characterize the mechanics of oil droplet capture, transport and ingestion by benthic ciliary filter feeders, and contribute to understanding the behavior of animals in response to oil emulsions, and how oils enter marine food webs.

Enteropneusts (acorn worms) are hemichordates, the sister group to echinoderms. Together they form the clade Ambulacraria, which is closely related to chordates. All three groups appear in the lower Cambrian, but their interrelationships remain problematic, which impedes the understanding of early deuterostome evolution. Enteropneusts are also extremely rare in the fossil record, only a few species are known from Lagerstatten-type deposits. Here, we describe the earliest known enteromens, including tornaria larvae and juveniles, from the lower Cambrian (Epoch 2, Stage 3) Haiyan Lagerstatte, Chengjiang biota, of China. The enteropneust larvae and post-metamorphic juveniles are the first reported in the fossil record and provide direct evidence for a pelago-benthic lifestyle in a Cambrian deuterostome animal, bolstering the hypothesis that an indirect development is primitive to the enteropneusts and maybe the hemichordates or whole of Ambulacraria.

The gills are hypothesized to play a key role in early vertebrate evolution by replacing the skin as the primary site of gas exchange. In this scenario, water flow across the gills used for suspension feeding in ancestral deuterostomes was coopted for breathing in stem vertebrates to facilitate the evolution of larger, active fishes. This hypothesis is supported by a stem-vertebrate origin for structures that increase gill capacity for breathing. However, these structures might have instead enhanced an already dominant capacity at the gills of invertebrate deuterostomes rather than mark a shift from the skin. To test this, we characterized gill function for gas exchange in the suspension-feeding hemichordate acorn worm Protoglossus graveolens . We measured oxygen uptake and ammonia excretion in whole worms and worm halves with or without gills at 10°C and during an acute thermal challenge at 20°C to maximize gill recruitment. Gills did not enhance oxygen uptake or ammonia excretion, suggesting they are not a primary site of gas exchange. This is the first test of gill function for gas exchange in a suspension-feeding invertebrate deuterostome, and it provides essential support for the long-hypothesized vertebrate origin of breathing at gills and its role in early vertebrate evolution.### Competing Interest StatementThe authors have declared no competing interest.

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.

Various methods of oil spill remediation exist, e.g., floating booms, controlled burning and the release of chemical surfactants. These surfactants facilitate the breakup of the slick into micron-sized droplets. Here, we studied the impact such a surfactant has on the size distribution of oil droplets in the water column and in the gut of the filter feeder Daphnia magna. We also studied the effect of surfactants on detachment conditions of chemically and mechanically dispersed oil (respectively MDO and CDO) droplets from capture fibers. Our results show that including solubilized dioctyl sulfosuccinate sodium salt in the mixing of the emulsion produces smaller droplets and a narrower size distribution in the water. In the gut, the size of ingested droplets does not change whether the oil is mixed mechanically or chemically. Also, surfactant coated droplets detach at a lower velocity than mechanically dispersed droplet because of their lower oil/water interfacial tension.

AbstractThe gills are hypothesized to play a key role in early vertebrate evolution by replacing the skin as the primary site of gas exchange. In this scenario, water flow across the gills used for suspension feeding in ancestral deuterostomes was coopted for breathing in stem vertebrates to facilitate the evolution of larger, active fishes. This hypothesis is supported by a stem-vertebrate origin for structures that increase gill capacity for breathing. However, these structures might have instead enhanced an already dominant capacity at the gills of invertebrate deuterostomes rather than mark a shift from the skin. To test this, we characterized gill function for gas exchange in the suspension-feeding hemichordate acorn wormProtoglossus graveolens. We measured oxygen uptake and ammonia excretion in whole worms and worm halves with or without gills at 10°C and during an acute thermal challenge at 20°C to maximize gill recruitment. Gills did not enhance oxygen uptake or ammonia excretion, suggesting they are not a primary site of gas exchange. This is the first test of gill function for gas exchange in a suspension-feeding invertebrate deuterostome, and it provides essential support for the long-hypothesized vertebrate origin of breathing at gills and its role in early vertebrate evolution.

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.

Deuterostomes comprise three phyla with radically different body plans. Phylogenetic bracketing of the living deuterostome clades suggests the latest common ancestor of echinoderms, hemichordates and chordates was a bilaterally symmetrical worm with pharyngeal openings, with these characters lost in echinoderms. Early fossil echinoderms with pharyngeal openings have been described, but their interpretation is highly controversial. Here, we critically evaluate the evidence for pharyngeal structures (gill bars) in the extinct stylophoran echinoderms Lagynocystis pyramidalis and Jaekelocarpus oklahomensis using virtual models based on high-resolution X-ray tomography scans of three-dimensionally preserved fossil specimens. Multivariate analyses of the size, spacing and arrangement of the internal bars in these fossils indicate they are substantially more similar to gill bars in modern enteropneust hemichordates and cephalochordates than to other internal bar-like structures in fossil blastozoan echinoderms. The close similarity between the internal bars of the stylophorans L. pyramidalis and J. oklahomensis and the gill bars of extant chordates and hemichordates is strong evidence for their homology. Differences between these internal bars and bar-like elements of the respiratory systems in blastozoans suggest these structures might have arisen through parallel evolution across deuterostomes, perhaps underpinned by a common developmental genetic mechanism.

Gas exchange and ion regulation at gills have key roles in the evolution of vertebrates 1 – 4 . Gills are hypothesized to have first acquired these important homeostatic functions from the skin in stem vertebrates, facilitating the evolution of larger, more-active modes of life 2 , 3 , 5 . However, this hypothesis lacks functional support in relevant taxa. Here we characterize the function of gills and skin in a vertebrate (lamprey ammocoete; Entosphenus tridentatus ), a cephalochordate (amphioxus; Branchiostoma floridae ) and a hemichordate (acorn worm; Saccoglossus kowalevskii ) with the presumed burrowing, filter-feeding traits of vertebrate ancestors 6 – 9 . We provide functional support for a vertebrate origin of gas exchange at the gills with increasing body size and activity, as direct measurements in vivo reveal that gills are the dominant site of gas exchange only in ammocoetes, and only with increasing body size or challenges to oxygen supply and demand. Conversely, gills of all three taxa are implicated in ion regulation. Ammocoete gills are responsible for all ion flux at all body sizes, whereas molecular markers for ion regulation are higher in the gills than in the skin of amphioxus and acorn worms. This suggests that ion regulation at gills has an earlier origin than gas exchange that is unrelated to vertebrate size and activity—perhaps at the very inception of pharyngeal pores in stem deuterostomes.

Crustacean filter feeders capture oil droplets with the use of their ramified appendages. These appendages behave as paddles or sieves, based on the system's Reynolds number. Here, we used high-speed videography, scanning electron microscopy and fluid mechanics to study the capturing mechanisms of crude oil droplets and the filtering appendage's wettability by two species of barnacles (Balanus glandula and Balanus crenatus) and of the freshwater cladoceran Daphnia magna. Our results show that barnacle appendages behave as paddles and capture droplets in their boundary layers at low Reynolds number. At high Reynolds number, droplets are most likely to be captured via direct interception. There is an intermediate range of Reynolds number where droplets can be captured by both mechanisms at the same time. Daphnia magna captures droplets in the boundary layers of the third and fourth pair of thoracic legs with a metachronal motion of the appendages. All studied surfaces were revealed to be highly lipophobic, demonstrating captured oil droplets with high contact angles. We also discuss implications of such capture mechanisms and wettability on potential ingestion of crude oil by filter feeders. These results further our understanding of the capture of crude oil by filter feeders, shedding light on the main entry point of oil in marine food webs.

The extant graptolite Rhabdopleura recondita has been so far recorded only as inhabiting a bryozoan skeleton. Its larval settlement and metamorphosis are possible in the absence of a bryozoan zoarium, whereas further colony development may require that the larva is hidden inside the bryozoan host. This dependence may constrain the development of R. recondita tube and tubaria compared to the other Rhabdopleura species that develop without a host. We report here on larval settlement and metamorphosis in the absence/presence of a bryozoan host skeleton. We also make the first attempt to test the phenotypical response of R. recondita tubes and tubaria under variable hydrodynamic regimes in laboratory conditions. After 40 days, no significant variation was detected in the number or length of the newly formed tubes. These findings suggest that R. recondita eventually resides in a narrow velocity range and that tube and tubarium development is largely invariable.

Pterobranchs originated in the basal Cambrian (Fortunian) and are mostly known by their tubes preserved in the fossil record. The earliest forms are represented by bushy erect growing colonies that are not widely studied due to their scarcity, preservation quality and species misidentification. For this reason, early phylogenetic relationships within the group are not clearly established. Middle Cambrian Burgess Shale graptolites were poorly known, based on the presence of Chaunograptus scandens, some debatable species of the genus Yuknessia, and other undetermined fragmented material. This study represents a complete description of C. scandens, a consensus for Yuknessia simplex and Y. stephenensis, and new reports of Protohalecium hallianum and Mastigograptus sp. from the Burgess Shale localities, which have also been found in other Burgess Shale type localities in Utah and Australia. Phylogenetic analyses of 34 discrete morphological traits from these Burgess Shale genera and some known benthic and planktic taxa (n = 22), place these Cambrian species as basal forms closer to the pseudocolonial pterobranch Cephalodiscus and the living graptolite Rhabdopleura.

Hemichordate relationships remain contentious due to conflicting molecular results [1-7] and the high degree ofmorphological disparity between the two hemichordate classes, Enteropneusta and Pterobranchia [8-11]. Additionally, hemichordates have a poor fossil record outside of the Cambrian, with the exception of the collagenous tubes of the pterobranchs (which include graptolites). By the middle Cambrian, tube-dwelling colonial pterobranchs [12, 13] and tube-dwelling enteropneusts coexisted [14, 15], supporting the origin of the hemichordate body plan earlier in the Cambrian without clarifying the morphology of their last common ancestor. Here, we describe a new hemichordate, Gyaltsenglossus senis, based on 33 specimens from the 506-million-year-old Burgess Shale (Odaray Mountain, British Columbia). G. senis has a unique combination of soft anatomical characters found in both extant classes of hemichordates, namely a trimeric-vermiform body plan with an elongate proboscis and six feeding arms with tentacles. The trunk possesses a long through-gut and terminates with a bulbous structure potentially used for locomotion and/or as a temporary anchor. There is no evidence of a secreted tube. Our phylogenetic analyses retrieve this newtaxon as a stemgroup hemichordate, supporting the hypothesis that a vermiform body plan preceded both tube building and colonial ecologies. This new taxon suggests that a bimodal feeding ecology using tentacles to filter feed and a proboscis to deposit feed may be plesiomorphic in hemichordates. Finally, the presence of a muscular, post-anal attachment structure in all known Cambrian hemichordates supports this feature as an additional hemichordate plesiomorphy critical for understanding early hemichordate evolution.

AbstractWe measured gill slit fluctuating asymmetry (FA), a measure of developmental noise, in adults of three invertebrate deuterostomes with different feeding modes: the cephalochordateBranchiostoma floridae(an obligate filter feeder), the enteropneustsProtoglossus graveolens(a facultative filter feeder/deposit feeder) andSaccoglossus bromophenolosus(a deposit feeder). FA was substantially and significantly low inB. floridaeandP. graveolensand high inS. bromophenolosus. Our results suggest that the gills of species that have experienced a relaxation of the filter feeding trait exhibit elevated FA. We found that the timing of development of the secondary collagenous gill bars, compared to the primary gill bars, was highly variable inP. graveolensbut not the other two species, demonstrating an independence of gill FA from gill bar heterochrony. We also discovered the occasional ectopic expression of a second set of paired gills posterior to the first set of gills in the enteropneusts and that these were more common inS. bromophenolosus. Moreover, our finding that gill slits in enteropneusts exhibit bilateral symmetry suggests that the left‐sidedness of larval cephalochordate gills, and the directional asymmetry of Cambrian stylophoran echinoderm fossil gills, evolved independently from a bilaterally symmetrical ancestor.

Rhabdopleura Allman, 1869 is one of the longest surviving animal genera. The five-known species are the only living Graptolithina, a group well known from their diverse Paleozoic fossil record. Here we add information on the soft-bodied zooids and molecular phylogenetics of Rhabdopleura annulata Norman, 1921, which was previously only known from its tubes. Tubes and zooids were collected from Heron Island, Queensland, Australia. Zooids have a single pair of tentaculated arms. Dark pigment granules are found throughout the body, and particularly dense in the pair of arms and the anterior lip of the cephalic shield. Colonies grow encrusted in and on coral debris. The tubes are either creeping or erect, but no stolon has been found. Inside of the coral matrix lacunae, the tube cortex formed a parchment-like wallpaper. Phylogenetic analysis based on combined 18S+16S rRNA sequences placed R. annulata as sister to the remaining rhabdopleurids, albeit with weak support. The biogeographic range of R. annulata extends from Indonesia to Tasmania, and New Zealand. Its occurrence on Heron Island does not extend this range, but highlights that rhabdopleurids may be more common, and in shallower waters, than previously appreciated, permitting further studies that may shed light on graptolite paleobiology.