Immunohistochemical investigations of the development of <i>Scoloplos armiger</i> (“intertidalis clade”) indicate a paedomorphic origin of <i>Proscoloplos cygnochaetus</i> (Annelida, Orbiniidae)

Helm, Conrad; Krause, Anne; Bleidorn, Christoph

doi:10.1111/ivb.12090

Cited by 7 publications

(4 citation statements)

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“…A limited number of studies dealing with nervous system development in Annelida (including Sipuncula) shows that the subepidermal annelid VNC develops from a larval intraepidermal ventral cord [ 21 , 66 , 68 ]. Our analyses (Figs.…”

Section: Resultsmentioning

confidence: 99%

Convergent evolution of the ladder-like ventral nerve cord in Annelida

et al. 2018

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BackgroundA median, segmented, annelid nerve cord has repeatedly been compared to the arthropod and vertebrate nerve cords and became the most used textbook representation of the annelid nervous system. Recent phylogenomic analyses, however, challenge the hypothesis that a subepidermal rope-ladder-like ventral nerve cord (VNC) composed of a paired serial chain of ganglia and somata-free connectives represents either a plesiomorphic or a typical condition in annelids.ResultsUsing a comparative approach by combining phylogenomic analyses with morphological methods (immunohistochemistry and CLSM, histology and TEM), we compiled a comprehensive dataset to reconstruct the evolution of the annelid VNC. Our phylogenomic analyses generally support previous topologies. However, the so far hard-to-place Apistobranchidae and Psammodrilidae are now incorporated among the basally branching annelids with high support. Based on this topology we reconstruct an intraepidermal VNC as the ancestral state in Annelida. Thus, a subepidermal ladder-like nerve cord clearly represents a derived condition.ConclusionsBased on the presented data, a ladder-like appearance of the ventral nerve cord evolved repeatedly, and independently of the transition from an intraepidermal to a subepidermal cord during annelid evolution. Our investigations thereby propose an alternative set of neuroanatomical characteristics for the last common ancestor of Annelida or perhaps even Spiralia.Electronic supplementary materialThe online version of this article (10.1186/s12983-018-0280-y) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Convergent evolution of the ladder-like ventral nerve cord in Annelida

et al. 2018

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“…5 and 6 ), whereas earlier stages only showed aTub-LIR in cilia. Such a developmental pattern with neuropeptide immunoreactivity arising early in the apical organ, the circumesophageal connectives and the anterior stomatogastric nervous system is well-known in other lophotrochozoans, such as the errant annelids Platynereis dumerilli [ 22 ] and Phyllodoce groenlandica [ 44 ], the sedentary annelids Sabellaria alveolata [ 20 ], Capitella teleta [ 9 , 45 ] and Scoloplos armiger [ 25 ], sipunculids [ 21 ] and aplacophoran molluscs [ 46 ]. The absence of serotonergic somata in the apical organ of the early stages of O. fusiformis differs from the situation in most lophotrochozoans, such as Annelida, Mollusca, Entoprocta, and Platyhelminthes, where prominent apical flask-shaped neurons showing 5-HT-LIR (and FMRFamide-LIR) appear early in the development [ 20 , 24 , 46 – 49 ].…”

Section: Resultsmentioning

confidence: 99%

Owenia fusiformis – a basally branching annelid suitable for studying ancestral features of annelid neural development

et al. 2016

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BackgroundComparative investigations on bilaterian neurogenesis shed light on conserved developmental mechanisms across taxa. With respect to annelids, most studies focus on taxa deeply nested within the annelid tree, while investigations on early branching groups are almost lacking. According to recent phylogenomic data on annelid evolution Oweniidae represent one of the basally branching annelid clades. Oweniids are thought to exhibit several plesiomorphic characters, but are scarcely studied - a fact that might be caused by the unique morphology and unusual metamorphosis of the mitraria larva, which seems to be hardly comparable to other annelid larva. In our study, we compare the development of oweniid neuroarchitecture with that of other annelids aimed to figure out whether oweniids may represent suitable study subjects to unravel ancestral patterns of annelid neural development. Our study provides the first data on nervous system development in basally branching annelids.ResultsBased on histology, electron microscopy and immunohistochemical investigations we show that development and metamorphosis of the mitraria larva has many parallels to other annelids irrespective of the drastic changes in body shape during metamorphosis. Such significant changes ensuing metamorphosis are mainly from diminution of a huge larval blastocoel and not from major restructuring of body organization. The larval nervous system features a prominent apical organ formed by flask-shaped perikarya and circumesophageal connectives that interconnect the apical and trunk nervous systems, in addition to serially arranged clusters of perikarya showing 5-HT-LIR in the ventral nerve cord, and lateral nerves. Both 5-HT-LIR and FMRFamide-LIR are present in a distinct nerve ring underlying the equatorial ciliary band. The connections arising from these cells innervate the circumesophageal connectives as well as the larval brain via dorsal and ventral neurites. Notably, no distinct somata with 5-HT -LIR in the apical organ are detectable in the larval stages of Owenia.Most of the larval neural elements including parts of the apical organ are preserved during metamorphosis and contribute to the juvenile nervous system.ConclusionsOur studies in Owenia fusiformis strongly support that early branching annelids are comparable to other annelids with regard to larval neuroanatomy and formation of the juvenile nervous system. Therefore, Owenia fusiformis turns out to be a valuable study subject for comparative investigations and unravelling ancestral processes in neural development in Annelida and Bilateria in general.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0690-4) contains supplementary material, which is available to authorized users.

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“…Such presence of an adult-sized jaw apparatus in juveniles hints at a pedomorphic developmental mode for the mentioned structure in histriobdellids. Whether pedomorphosis is responsible for the observed developmental characteristics must be investigated in the future, but comparable processes are well documented for several annelid families [32][33][34].…”

Section: Discussionmentioning

confidence: 99%

New insights into the morphology and evolution of the ventral pharynx and jaws in Histriobdellidae (Eunicida, Annelida)

et al. 2020

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The jaw apparatus in several annelid families represents a powerful tool for systematic approaches and evolutionary investigations. Nevertheless, for several taxa, this character complex has scarcely been investigated, and complete comparative analyses of all annelid jaws are lacking. In our comprehensive study, we described the fine structure of the jaw apparatus and the ventral pharyngeal organ (VPO) in Histriobdella homari – a minute ectocommensal of lobsters putatively belonging to the Eunicida – using different comparative morphological approaches, including SEM, TEM, CLSM and subsequent 3D reconstruction. The H. homari jaw apparatus is composed of ventral paired mandibles and dorsal symmetrical maxillae consisting of numerous dental plates, ventral carriers and an unpaired dorsal rod, and the general assemblage and arrangement of the different parts are highly comparable to those of other eunicid families. The jaw ultrastructure of histriobdellids resembles that of the families Dorvilleidae and (juvenile) Onuphidae. Furthermore, our data reveal that in the process of development of the jaw apparatus, the mandibles, maxillae II and unpaired dorsal rod are formed first, and the remaining maxillae and ventral carriers appear later. Notably, the muscular apparatus differs from that in Dorvilleidae and Onuphidae in terms of the number and arrangement of muscle fibers encompassing the jaws – not only because of the very small size of Histriobdella but also because histriobdellid maxillary protraction occurs due to straightening of the dorsal rod and thus requires a different muscular scaffold. Based on our investigations, the arrangement of the muscular apparatus of the jaws, the presence of paired ventral carriers and the dorsal rod, and the morphology of the ventral pharyngeal organ represent a histriobdellid autapomorphy. Our datasets form a basis for further comparative analyses to elucidate the evolution of Eunicida and jaw-bearing Annelida.

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Immunohistochemical investigations of the development of Scoloplos armiger (“intertidalis clade”) indicate a paedomorphic origin of Proscoloplos cygnochaetus (Annelida, Orbiniidae)

Cited by 7 publications

References 59 publications

Convergent evolution of the ladder-like ventral nerve cord in Annelida

Convergent evolution of the ladder-like ventral nerve cord in Annelida

Owenia fusiformis – a basally branching annelid suitable for studying ancestral features of annelid neural development

New insights into the morphology and evolution of the ventral pharynx and jaws in Histriobdellidae (Eunicida, Annelida)

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