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Concept: Brachiopod

16

Evolutionary relationships among members of the Lophophorata remain unclear. Traditionally, the Lophophorata included three phyla: Brachiopoda, Bryozoa or Ectoprocta, and Phoronida. All species in these phyla have a lophophore, which is regarded as a homologous structure of the lophophorates. Because the organization of the nervous system has been traditionally used to establish relationships among groups of animals, information on the organization of the nervous system in the lophophore of phoronids, brachiopods, and bryozoans may help clarify relationships among the lophophorates. In the current study, the innervation of the lophophore of the inarticulate brachiopod Lingula anatina is investigated by modern methods. The lophophore of L. anatina contains three brachial nerves: the main, accessory, and lower brachial nerves. The main brachial nerve is located at the base of the dorsal side of the brachial fold and gives rise to the cross neurite bundles, which pass through the connective tissue and connect the main and accessory brachial nerves. Nerves emanating from the accessory brachial nerve account for most of the tentacle innervation and comprise the frontal, latero-frontal, and latero-abfrontal neurite bundles. The lower brachial nerve gives rise to the abfrontal neurite bundles of the outer tentacles. Comparative analysis revealed the presence of many similar features in the organization of the lophophore nervous system in phoronids, brachiopods, and bryozoans. The main brachial nerve of L. anatina is similar to the dorsal ganglion of phoronids and the cerebral ganglion of bryozoans. The accessory brachial nerve of L. anatina is similar to the minor nerve ring of phoronids and the circumoral nerve ring of bryozoans. All lophophorates have intertentacular neurite bundles, which innervate adjacent tentacles. The presence of similar nerve elements in the lophophore of phoronids, brachiopods, and bryozoans supports the homology of the lophophore and the monophyly of the lophophorates.

Concepts: Nervous system, Muscle, Axon, Nerve, Bryozoa, Ordovician, Brachiopod, Lophophore

15

Brachiopods are a lineage of invertebrates well known for the breadth and depth of their fossil record. While the quality of this fossil record attracts the attention of palaeontologists, geochemists and paleoclimatologists, modern day brachiopods are also of interest to evolutionary biologists due to their potential to address a variety of questions ranging from developmental biology to biomineralization. The brachiopod shell is a composite material primarily composed of either calcite or calcium phosphate in close association with proteins and polysaccharides which give these composite structures their material properties. The information content of these biomolecules, sequestered within the shell during its construction, have the potential to inform hypotheses focused on describing how brachiopod shell formation evolved. Here, using high throughput proteomic approaches and next generation sequencing, we have surveyed and characterized the first shell-proteome and shell-forming transcriptome of any brachiopod, the South American Magellania venosa (Rhynchonelliformea: Terebratulida). We find that the seven most abundant proteins present in the shell are unique to M. venosa, but that these proteins display biochemical features found in other metazoan biomineralization proteins. We can also detect some M. venosa proteins that display significant sequence similarity to other metazoan biomineralization proteins, suggesting that some elements of the brachiopod shell-forming proteome are deeply evolutionarily conserved. We also employed a variety of preparation methods to isolate shell proteins and find that in comparison to the shells of other spiralian invertebrates (such as molluscs) the shell ultrastructure of M. venosa may explain the affects these preparation strategies have on our results.

Concepts: DNA, Evolution, Molecular biology, Biology, Fossil, Paleontology, Calcite, Brachiopod

3

The diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids-distantly related animals considered to be segmented. Far less is known about the role of “segmentation genes” in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods-marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects-except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis.

Concepts: Organism, Species, Developmental biology, Arthropod, Annelid, Segmentation, Brachiopod, Modularity

2

Independent molecular and morphological phylogenetic analyses have often produced discordant results for certain groups which, for fossil-rich groups, raises the possibility that morphological data might mislead in those groups for which we depend upon morphology the most. Rhynchonellide brachiopods, with more than 500 extinct genera but only 19 extant genera represented today, provide an opportunity to explore the factors that produce contentious phylogenetic signal across datasets, as previous phylogenetic hypotheses generated from molecular sequence data bear little agreement with those constructed using morphological characters. Using a revised matrix of 66 morphological characters, and published ribosomal DNA sequences, we performed a series of combined phylogenetic analyses to identify conflicting phylogenetic signals. We completed a series of parsimony-based and Bayesian analyses, varying the data used, the taxa included, and the models used in the Bayesian analyses. We also performed simulation-based sensitivity analyses to assess whether the small size of the morphological data partition relative to the molecular data influenced the results of the combined analyses. In order to compare and contrast a large number of phylogenetic analyses and their resulting summary trees, we developed a measure for the incongruence between two topologies, and simultaneously ignore any differences in phylogenetic resolution. Phylogenetic hypotheses generated using only morphological characters differed amongst each other, and with previous analyses, while molecular-only and combined Bayesian analyses produced extremely similar topologies. Characters historically associated with traditional classification in the Rhynchonellida have very low consistency indices on the topology preferred by the combined Bayesian analyses. Overall, this casts doubt on the use of morphological systematics to resolve relationships among the crown rhynchonellide brachiopods. However, expanding our dataset to a larger number of extinct taxa with intermediate morphologies is necessary to exclude the possibility that the morphology of extant taxa is not dominated by convergence along long branches.

Concepts: DNA, Scientific method, Molecular biology, Sequence, Phylogenetics, Cladistics, Extinction, Brachiopod

1

The inability of organisms to cope in changing environments poses a major threat to their survival. Rising carbon dioxide concentrations, recently exceeding 400 μatm, are rapidly warming and acidifying our oceans. Current understanding of organism responses to this environmental phenomenon is based mainly on relatively short- to medium-term laboratory and field experiments, which cannot evaluate the potential for long-term acclimation and adaptation, the processes identified as most important to confer resistance. Here, we present data from a novel approach that assesses responses over a centennial timescale showing remarkable resilience to change in a species predicted to be vulnerable. Utilising museum collections allows the assessment of how organisms have coped with past environmental change. It also provides a historical reference for future climate change responses. We evaluated a unique specimen collection of a single species of brachiopod (Calloria inconspicua) collected every decade from 1900 to 2014 from one sampling site. The majority of brachiopod shell characteristics remained unchanged over the past century. One response, however, appears to reinforce their shell by constructing narrower punctae (shell perforations) and laying down more shell. This study indicates one of the most calcium-carbonate-dependent species globally to be highly resilient to environmental change over the last 120 years and provides a new insight for how similar species might react and possibly adapt to future change.

Concepts: Time, Carbon dioxide, Biology, Organism, Adaptation, Global warming, Carboniferous, Brachiopod

1

Shells of brachiopods are excellent archives for environmental reconstructions in the recent and distant past as their microstructure and geochemistry respond to climate and environmental forcings. We studied the morphology and size of the basic structural unit, the secondary layer fibre, of the shells of several extant brachiopod taxa to derive a model correlating microstructural patterns to environmental conditions. Twenty-one adult specimens of six recent brachiopod species adapted to different environmental conditions, from Antarctica, to New Zealand, to the Mediterranean Sea, were chosen for microstructural analysis using SEM, TEM and EBSD. We conclude that: 1) there is no significant difference in the shape and size of the fibres between ventral and dorsal valves, 2) there is an ontogenetic trend in the shape and size of the fibres, as they become larger, wider, and flatter with increasing age. This indicates that the fibrous layer produced in the later stages of growth, which is recommended by the literature to be the best material for geochemical analyses, has a different morphostructure and probably a lower organic content than that produced earlier in life. In two species of the same genus living in seawater with different temperature and carbonate saturation state, a relationship emerged between the microstructure and environmental conditions. Fibres of the polar L. uva tend to be smaller, rounder and less convex than those of the temperate L. neozelanica, suggesting a relationship between microstructural size, shell organic matter content, ambient seawater temperature and calcite saturation state.

Concepts: Mediterranean Sea, Fiber, Shell, Dietary fiber, Environmental science, Calcite, Shell, Wyoming, Brachiopod

1

An anomalocaridid from the Ordovician exposes a second set of body flaps and reopens the question of how the two branches of arthropod legs evolved.

Concepts: Cambrian explosion, Brachiopod, Evolutionary history of life

1

Lobopodians, a nonmonophyletic assemblage of worm-shaped soft-bodied animals most closely related to arthropods, show two major morphotypes: long-legged and short-legged forms. The morphotype with stubby, conical legs has a long evolutionary history, from the early Cambrian [1] through the Carboniferous [2, 3], including the living onychophorans and tardigrades [4-6]. Species with tubular lobopods exceeding the body diameter have been reported exclusively from the Cambrian [7-12]; the three-dimensionally preserved Orstenotubulus evamuellerae from the uppermost middle Cambrian “Orsten” (Sweden) is the youngest long-legged lobopodian reported thus far [8]. Here we describe a new long-legged lobopodian, Carbotubulus waloszeki gen. et sp. nov., from Mazon Creek, Illinois, USA (∼296 million years ago) [13]. This first post-Cambrian long-legged lobopodian extends the range of this morphotype by about 200 million years. The three-dimensionally preserved specimen differs significantly from the associated short-legged form Ilyodes inopinata [2], of which we also present new head details. The discovery of a Carboniferous long-legged lobopodian provides a more striking example of the long-term survival of Cambrian morphotypes than, for example, the occurrence of a Burgess Shale-type biota in the Ordovician of Morocco [14] and dampens the effect of any major extinction of taxa at the end of the middle Cambrian [15, 16].

Concepts: Evolution, Arthropod, Extinction event, Ordovician, Trilobite, Cambrian, Brachiopod, Mazon River

0

Phylum Brachiopoda, shelled marine invertebrates, is currently represented by about 400 extant species; a tiny fraction of the ca. 30,000 described fossil species (Emig et al. 2013; Bitner 2014; Nauendorf et al. 2014; Logan et al. 2015). Only twenty of these Recent species are known from the Chilean coasts (Lee et al. 2008), most of them from subtidal waters. Of these, only Magellania venosa (Dixon, 1789) (the largest extant brachiopod) and Discinisca lamellosa (Broderip, 1833) are common species found in the southern and central-northern coasts of the country, respectively. As with other marine invertebrates, brachiopods from the region have been reviewed in few studies, apart from some classic nineteenth century works by Sowerby (1822); Broderip (1833); Davidson (1878, 1888); Dall (1895, 1902, 1908), and by Dall and Pilsbry (1891). More recent studies include Cooper (1973, 1982) and Foster (1989) reviewing brachiopods from the Southern Hemisphere and the extreme South Pacific; Zezina (1981, 1989) describing species from the underwater ridges of the Eastern Pacific; Moyano (1995) who revised all the literature dealing with Brachiopoda in Chile; and most recently Baumgarten et al. (2014) who studied the population structure of Magellania venosa in the fjord region of southern Chile.

Concepts: Arthropod, Pacific Ocean, Annelid, Paleontology, Calcite, Brachiopod, Devonian, 1908

0

Brachiopod shells are the most widely used geological archive for the reconstruction of the temperature and the oxygen isotope composition of Phanerozoic seawater. However, it is not conclusive whether brachiopods precipitate their shells in thermodynamic equilibrium. In this study, we investigated the potential impact of kinetic controls on the isotope composition of modern brachiopods by measuring the oxygen and clumped isotope compositions of their shells. Our results show that clumped and oxygen isotope compositions depart from thermodynamic equilibrium due to growth rate-induced kinetic effects. These departures are in line with incomplete hydration and hydroxylation of dissolved CO2. These findings imply that the determination of taxon-specific growth rates alongside clumped and bulk oxygen isotope analyses is essential to ensure accurate estimates of past ocean temperatures and seawater oxygen isotope compositions from brachiopods.

Concepts: Oxygen, Energy, Temperature, Thermodynamics, Heat, Calcite, Thermodynamic equilibrium, Brachiopod