Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

Baeumler, Natalie; Haszprunar, Gerhard; Ruthensteiner, Bernhard

doi:10.1186/1742-9994-9-23

Cited by 12 publications

(7 citation statements)

References 33 publications

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“…The excretory organ of Helminthope resembles the paired larval/juvenile nephridia described recently in the chiton Lepidochitona Gray, 1821 [67,68]: these possess ‘larval’ protonephridia (with filter zone and vacuolated part) that become fully reduced, and ‘early adult’ protonephridia with an originally similar morphology that later becomes modified to form a metanephridial system after joining the pericardium. We assume that this mechanism is similar in heterobranch gastropods, including rhodopemorphs that possess only the (right) kidney as adults.…”

Section: Discussionmentioning

confidence: 92%

“…As discussed above, the configuration of ganglia in Helminthope (except for the accessory ganglia) is highly similar to what Riedl [35] observed in 13 days old Rhodope , with still unfused visceral loop ganglia spread along the longitudinal body axis. Also, the lack of a heart (in mollusks developed shortly before metamorphosis, [108]) and therefore presence of only a protonephridial-type kidney (present before the heart; [68]) are early ontogenetic characters persisting in the adult. While heterobranchs are hypothesized to have evolved from an apogastropod ancestor in the centimeter size range by progenetic miniaturization and simplification especially of digestive and mantle cavity organs [18], rhodopemorphs have reduced body complexity even further parallel to their invasion of meiofaunal habitats accompanied by progenesis.…”

Section: Discussionmentioning

confidence: 99%

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At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

2013

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BackgroundGastropods are among the most diverse animal clades, and have successfully colonized special habitats such as the marine sand interstitial. Specialized meiofaunal snails and slugs are tiny and worm-shaped. They combine regressive features – argued to be due to progenetic tendencies – with convergent adaptations. Microscopic size and concerted convergences make morphological examination non-trivial and hamper phylogenetic reconstructions. The enigmatic turbellarian-like Rhodopemorpha are a small group that has puzzled systematists for over a century. A preliminary molecular framework places the group far closer to the root of Heterobranchia – one of the major gastropod groups – than previously suggested. The poorly known meiofaunal Helminthope psammobionta Salvini-Plawen, 1991 from Bermuda is the most worm-shaped free-living gastropod and shows apparently aberrant aspects of anatomy. Its study may give important clues to understand the evolution of rhodopemorphs among basal heterobranchs versus their previously thought origin among ‘higher’ euthyneuran taxa.ResultsWe describe the 3D-microanatomy of H. psammobionta using three-dimensional digital reconstruction based on serial semithin histological sections. The new dataset expands upon the original description and corrects several aspects. Helminthope shows a set of typical adaptations and regressive characters present in other mesopsammic slugs (called ‘meiofaunal syndrome’ herein). The taxonomically important presence of five separate visceral loop ganglia is confirmed, but considerable further detail of the complex nervous system are corrected and revealed. The digestive and reproductive systems are simple and modified to the thread-like morphology of the animal; the anus is far posterior. There is no heart; the kidney resembles a protonephridium. Data on all organ systems are compiled and compared to Rhodope.ConclusionsHelminthope is related to Rhodope sharing unique apomorphies. We argue that the peculiar kidney, configuration of the visceral loop and simplicity or lack of other organs in Rhodopemorpha are results of progenesis. The posterior shift of the anus in Helminthope is interpreted as a peramorphy, i.e. hypertrophy of body length early in ontogeny. Our review of morphological and molecular evidence is consistent with an origin of Rhodopemorpha slugs among shelled ‘lower Heterobranchia’. Previously thought shared ‘diagnostic’ features such as five visceral ganglia are either plesiomorphic or convergent, while euthyneury and a double-rooted cerebral nerve likely evolved independently in Rhodopemorpha and Euthyneura.

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

2013

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“…Another frequently applied method of combining LM with TEM in the same specimen is alternating LM and TEM sectioning. Our own experience [23,24] has shown that LM re-sectioning is much more efficient, because alternating sectioning requires repeated changes of the equipment (e.g. knife, microtome) during sectioning and the number of sections to be examined with the TEM is significantly higher.…”

Section: Discussionmentioning

confidence: 99%

“…The muscular, vascular, excretory, and digestive systems were chosen for segmentation and surface rendering. The excretory organs were selected for the TEM investigation because their size relative to the entire specimen is typical for fine structural investigations, they bear complex ultrastructural details, and their detailed organization contributes information to ongoing studies on the nephrogenesis of molluscs [23,24]. …”

Section: Introductionmentioning

confidence: 99%

A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario

et al. 2013

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BackgroundIn biomedical research, a huge variety of different techniques is currently available for the structural examination of small specimens, including conventional light microscopy (LM), transmission electron microscopy (TEM), confocal laser scanning microscopy (CLSM), microscopic X-ray computed tomography (microCT), and many others. Since every imaging method is physically limited by certain parameters, a correlative use of complementary methods often yields a significant broader range of information. Here we demonstrate the advantages of the correlative use of microCT, light microscopy, and transmission electron microscopy for the analysis of small biological samples.ResultsWe used a small juvenile bivalve mollusc (Mytilus galloprovincialis, approximately 0.8 mm length) to demonstrate the workflow of a correlative examination by microCT, LM serial section analysis, and TEM-re-sectioning. Initially these three datasets were analyzed separately, and subsequently they were fused in one 3D scene. This workflow is very straightforward. The specimen was processed as usual for transmission electron microscopy including post-fixation in osmium tetroxide and embedding in epoxy resin. Subsequently it was imaged with microCT. Post-fixation in osmium tetroxide yielded sufficient X-ray contrast for microCT imaging, since the X-ray absorption of epoxy resin is low. Thereafter, the same specimen was serially sectioned for LM investigation. The serial section images were aligned and specific organ systems were reconstructed based on manual segmentation and surface rendering. According to the region of interest (ROI), specific LM sections were detached from the slides, re-mounted on resin blocks and re-sectioned (ultrathin) for TEM. For analysis, image data from the three different modalities was co-registered into a single 3D scene using the software AMIRA®. We were able to register both the LM section series volume and TEM slices neatly to the microCT dataset, with small geometric deviations occurring only in the peripheral areas of the specimen. Based on co-registered datasets the excretory organs, which were chosen as ROI for this study, could be investigated regarding both their ultrastructure as well as their position in the organism and their spatial relationship to adjacent tissues. We found structures typical for mollusc excretory systems, including ultrafiltration sites at the pericardial wall, and ducts leading from the pericardium towards the kidneys, which exhibit a typical basal infolding system.ConclusionsThe presented approach allows a comprehensive analysis and presentation of small objects regarding both the overall organization as well as cellular and subcellular details. Although our protocol involves a variety of different equipment and procedures, we maintain that it offers savings in both effort and cost. Co-registration of datasets from different imaging modalities can be accomplished with high-end desktop computers and offers new opportunities for understanding and communicating structural relatio...

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“…A espécie Leptochiton darioi (Righi, 1973) Heath (1905), Ashby (1929), Yonge (1932), Fretter (1938), Graham (1973, Boyle (1975Boyle ( ), ᴓkland (1980, Baxter & Jones (1981), Fischer (1988, Russel-Hunter (1988), Wanninger & Haszprunar (2002), Saito (2003), Sigwart (2008Sigwart ( , 2009, Vendrasco et al (2008), Schwabe (2010), Kodirov (2011), Baeumler (2012, Sigwart et al (2013Sigwart et al ( , 2014, Sigwart & Schwabe (2017).…”

Section: Seleção Dos Terminaismentioning

confidence: 99%

Revisão taxonômica e filogenia da subfamília Callistoplacinae (Mollusca: Polyplacophora: Chitonoidea)

Gomes¹

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Agradeço ao Prof. Dr. Luiz R. L. de Simone pela orientação. O presente trabalho foi realizado com apoio da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES) -Código de financiamento 001. Ao Museu de Zoologia pelos amigos e momentos especiais que pude vivenciar. Aos meus familiares. Muito Obrigado! "É melhor morrer de pé do que viver de joelhos" -Emiliano Zapata Resumo A análise cladística de Callistoplacinae (Callistochitonidae) é apresentada com base em 175 caracteres e 39 espécies. O suporte de Callistoplacinae é corroborada por diferentes estudos baseados em dados tradicionais e a elevação a nível de família de Callistochitonidae é recuperada. Callistoplacinae compreende um gênero com seis espécies. Os dados morfológicos subsidiam uma nova proposta filogenética em que os então reconhecidos gêneros Calloplax e Ischnoplax passa a ser Callistoplax visando manter a estabilidade nomenclatural do grupo. Palavras-chave: Callistochitonidae. Callistoplacinae. Morfologia. Filogenia. anatomia.

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Development of the excretory system in a polyplacophoran mollusc: stages in metanephridial system development

Cited by 12 publications

References 33 publications

At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario

Revisão taxonômica e filogenia da subfamília Callistoplacinae (Mollusca: Polyplacophora: Chitonoidea)

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