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Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system.

ABSTRACT: BACKGROUND: Metamorphic remodeling of the nervous system and its organization in juvenile may shed light on early steps of evolution and can be used as an important criterion for establishing the relationships among large groups of animals. The protostomian affiliation of phoronids does not still have certain morphological and embryological proofs. In addition, the relationship of phoronids and other former "lophophorates" is still uncertain. The resolving of these conflicts requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri. RESULTS: During metamorphosis, the juvenile consumes the nerve elements of the larval hood. Two dorsolateral groups of larval perikarya remain and give rise to the dorsal ganglion, which appears as the "commissural brain". The juvenile inherits the main and minor tentacular nerve rings from the larva. Although the larval tentacles are directly inherited by the juvenile in P. harmeri, the ultrastructure and location of the definitive tentacular neurite bundles change greatly. Innervation of the juvenile lophophore exhibits a regular alternation of the intertentacular and abfrontal neurite bundles. The giant nerve fiber appears at early stage of metamorphosis and passes from the right group of dorsolateral perikarya to the left side of the body. DISCUSSION: THE METAMORPHIC REMODELING OF THE PHORONID NERVOUS SYSTEM OCCURS IN TWO DIFFERENT WAYS: with complete or incomplete destruction of organ systems. The morphology of the lophophore seems similar to those of the former members of "Lophophorata", but its innervation differs greatly. These findings support the separation of bryozoans from Lophophorata and establish a need for new data on the organization of the brachiopod nervous system. The nervous system of the phoronid juvenile is organized as an epidermal nerve plexus but exhibits a nerve center in the anterior portion of the body. The simultaneous presence of both the apical organ and anlage of the cerebral ganglion in phoronids at the larval stage, and the reduction of the apical organ during metamorphosis support the Trochea theory and allow to suggest the presence of two nervous centers in the last common ancestor of the Bilateria. Phoronids retained some plesiomorphic traits and can be regarded as one of the most primitive groups of lophotrochozoans.

SUBMITTER: Temereva EN

PROVIDER: S-EPMC4026883 | biostudies-other | 2014

REPOSITORIES: biostudies-other

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Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system.

Temereva Elena N EN Tsitrin Eugeni B EB

Frontiers in zoology 20140428

<h4>Background</h4>Metamorphic remodeling of the nervous system and its organization in juvenile may shed light on early steps of evolution and can be used as an important criterion for establishing the relationships among large groups of animals. The protostomian affiliation of phoronids does not still have certain morphological and embryological proofs. In addition, the relationship of phoronids and other former "lophophorates" is still uncertain. The resolving of these conflicts requires deta ...[more]

PMID: 24847374

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Project description:BackgroundThe organization and development of the nervous system has traditionally been used as an important character for establishing the relationships among large groups of animals. According to this criterion, phoronids were initially regarded as deuterostomian but have more recently been regarded as protostomian. The resolving of this conflict requires detailed information from poorly investigated members of phoronids, such as Phoronopsis harmeri.ResultsThe serotonin-like immunoreactive part of the P. harmeri nervous system changes during larval development. These changes mostly concern the nervous system of the hood and correlate with the appearance of the median and two marginal neurite bundles, the frontal organ, and the sensory field. The apical organ has bilateral symmetry. The tentacular neurite bundle passes under the tentacles, contains several types of perikarya, and gives rise to intertentacular bundles, which branch in the tentacle base and penetrate into adjacent tentacles by two lateroabfrontal bundles. There are two groups of dorsolateral perikarya, which exhibit serotonin-like immunoreactivity, contact the tentacular neurite bundle, and are located near the youngest tentacles. Larvae have a minor nerve ring, which originates from the posterior marginal neurite bundle of the hood, passes above the tentacle base, and gives rise to the mediofrontal neurite bundle in each tentacle. Paired laterofrontal neurite bundles of tentacles form a continuous nerve tract that conducts to the postoral ciliated band.DiscussionThe organization of the nervous system differs among the planktotrophic larvae of phoronid species. These differences may correlate with differences in phoronid biology. Data concerning the innervation of tentacles in different phoronid larvae are conflicting and require careful reinvestigation. The overall organization of the nervous system in phoronid larvae has more in common with the deuterostomian than with the protostomian nervous system. Phoronid larvae demonstrate some "deuterostome-like" features, which are, in fact, have to be ancestral bilaterian characters. Our new results and previous data indicate that phoronids have retained some plesiomorphic features, which were inherited from the last common ancestor of all Bilateria. It follows that phoronids should be extracted from the Trochozoan (=Spiralia) clade and placed at the base of the Lophotrochozoan stem.

Project description:The lophophore is a tentacle organ unique to the lophophorates. Recent research has revealed that the organization of the nervous and muscular systems of the lophophore is similar in phoronids, brachiopods, and bryozoans. At the same time, the evolution of the lophophore in certain lophophorates is still being debated. Innervation of the adult lophophore has been studied by immunocytochemistry and confocal laser scanning microscopy for only two brachiopod species belonging to two subphyla: Linguliformea and Rhynchonelliformea. Species from both groups have the spirolophe, which is the most common type of the lophophore among brachiopods. In this study, we used transmission electron microscopy, immunocytochemistry, and confocal laser scanning microscopy to describe the innervation of the most complex lophophore (the plectolophe) of the rhynchonelliform species Coptothyris grayi. The C. grayi lophophore (the plectolophe) is innervated by three brachial nerves: the main, second accessory, and lower. Thus, the plectolophe lacks the accessory brachial nerve, which is typically present in other studied brachiopods. All C. grayi brachial nerves contain two types of perikarya. Because the accessory nerve is absent, the cross nerves, which pass into the connective tissue, have a complex morphology: each nerve consists of two ascending and one descending branches. The outer and inner tentacles are innervated by several groups of neurite bundles: one frontal, two lateral, two abfrontal, and two latero-abfrontal (the latter is present in only the outer tentacles). Tentacle nerves originate from the second accessory and lower brachial nerves. The inner and outer tentacles are also innervated by numerous peritoneal neurites, which exhibit acetylated alpha-tubulin-like immunoreactivity. The nervous system of the lophophore of C. grayi manifests several evolutionary trends. On the one hand, it has undergone simplification, i.e., the absence of the accessory brachial nerve, which is apparently correlated with a reduction in the complexity of the lophophore's musculature. On the other hand, C. grayi has a prominent second accessory nerve, which contains large groups of frontal perikarya, and also has additional nerves extending from the both ganglia to the medial arm; these features are consistent with the complex morphology of the C. grayi plectolophe. In brachiopods, the evolution of the lophophore nervous system apparently involved two main modifications. The first modification was the appearance and further strengthening of the second accessory brachial nerve, which apparently arose because of the formation of a double row of tentacles instead of the single row of the brachiopod ancestor. The second modification was the partial or complete reduction of some brachial nerves, which was correlated with the reduced complexity of the lophophore musculature and the appearance of skeletal structures that support the lophophore.

Project description:One of the biggest challenges in biology is to understand how activity at the cellular level of neurons, as a result of their mutual interactions, leads to the observed behavior of an organism responding to a variety of environmental stimuli. Investigating the intermediate or mesoscopic level of organization in the nervous system is a vital step towards understanding how the integration of micro-level dynamics results in macro-level functioning. The coordination of many different co-occurring processes at this level underlies the command and control of overall network activity. In this paper, we have considered the somatic nervous system of the nematode Caenorhabditis elegans, for which the entire neuronal connectivity diagram is known. We focus on the organization of the system into modules, i.e., neuronal groups having relatively higher connection density compared to that of the overall network. We show that this mesoscopic feature cannot be explained exclusively in terms of considerations such as, optimizing for resource constraints (viz., total wiring cost) and communication efficiency (i.e., network path length). Even including information about the genetic relatedness of the cells cannot account for the observed modular structure. Comparison with other complex networks designed for efficient transport (of signals or resources) implies that neuronal networks form a distinct class. This suggests that the principal function of the network, viz., processing of sensory information resulting in appropriate motor response, may be playing a vital role in determining the connection topology. Using modular spectral analysis we make explicit the intimate relation between function and structure in the nervous system. This is further brought out by identifying functionally critical neurons purely on the basis of patterns of intra- and inter-modular connections. Our study reveals how the design of the nervous system reflects several constraints, including its key functional role as a processor of information.

Dataset Information

Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system.

Publications

Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system.

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