Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

Nielsen, Claus

doi:10.1002/jez.b.20001

Cited by 136 publications

(184 citation statements)

References 147 publications

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“…Greater similarities are found among nonfeeding larval forms within the Lophotrochozoa, particularly in the development and morphology of large multiciliated cells used for propulsion. Similar numbers (16) and arrangements of what appear to be primary trochoblast-like cell groups are found during the development the nonfeeding larval forms of kamptozoans (Barrois, 1877;Nielsen, 2005), nemerteans (Maslakova et al, 2004b), bryozoans (Barrois, 1877), and many trochophore larval types (albeit prototrochal cells bear compound cilia, see Nielsen, 2004Nielsen, , 2005. Considering the embryological origin (Zimmer, 1997) and functional plasticity of ciliated cells within bryozoan larvae, it is probable that the morphological similarities shared among the coronal cells of bryozoan larvae and the prototrochal cells of spiralians are the result of convergent functional solutions to swimming in the plankton (Emlet, 1994).…”

Section: Larval Morphology and Phylogenymentioning

confidence: 67%

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

Santagata

2007

Journal of Morphology

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Despite the embryological and anatomical disparities present among lophotrochozoan phyla, there are morphological similarities in the cellular arrangements of ciliated cells used for propulsion among the nonfeeding larval forms of kamptozoans, nemerteans, annelids, mollusks, and bryozoans. Evaluating whether these similarities are the result of convergent selective pressures or a shared (deep) evolutionary history is hindered by the paucity of detailed cellular information from multiple systematic groups from lesser-known, and perhaps, basal evolutionary phyla such as the Bryozoa. Here, I compare the ciliary fields and musculature among the major morphological grades of marine bryozoan larvae using light microscopy, SEM, and confocal imaging techniques. Sampling effort focused on six species from systematic groups with few published accounts, but an additional four well-known species were also reevaluated. Review of the main larval types among species of bryozoans and these new data show that, within select systematic groups of marine bryozoans, there is some conservation of the cellular arrangement of ciliary fields and larval musculature. However, there is much more morphological diversity in these structures than previously documented, especially among nonfeeding ctenostome larval types. This structural and functional diversification reflects species differences in the orientation of the apical disc during swimming and crawling behaviors, modification of the presumptive juvenile tissues, elongation of larval forms in the aboral-oral axis, maximizing the surface area of cell types with propulsive cilia, and the simplification of ciliary fields and musculature within particular lineages due to evolutionary loss. Considering the embryological origins and functional plasticity of ciliated cells within bryozoan larvae, it is probable that the morphological similarities shared between the coronal cells of bryozoan larvae and the prototrochal cells of trochozoans are the result of convergent functional solutions to swimming in the plankton. However, this does not rule out cell specification pathways shared by more closely related spiralian phyla. Overall, among the morphological grades of larval bryozoans, the structural variation and arrangement of the main cell groups responsible for ciliary propulsion have been evolutionarily decoupled from the more divergent modifications of larval musculature. The structure of larval ciliary fields reflects the functional demands of swimming and substrate exploration behaviors before metamorphosis, but this is in contrast to the morphology of larval musculature and presumptive juvenile tissues that are linked to macroevolutionary differences in morphogenetic movements during metamorphosis.

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Section: Larval Morphology and Phylogenymentioning

confidence: 67%

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

Santagata

2007

Journal of Morphology

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“…It furthermore reopens the debate about the putative ancestral segmentation of molluscs (3), because serial repetition of gills and pedal retractor muscles may be derived and not primitive features within molluscs. If this were the case, little evidence would remain for the case of homology of segmentation in annelids and serial repetition in molluscs (33), as confirmed in part by recent reevaluation of their early development (34,35).…”

Section: Resultsmentioning

confidence: 99%

Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons

Giribet

Okusu

Lindgren

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

197

117

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Monoplacophorans are among the rarest members of the phylum Mollusca. Previously only known from fossils since the Cambrian, the first living monoplacophoran was discovered during the famous second Galathea deep-sea expedition. The anatomy of these molluscs shocked the zoological community for presenting serially repeated gills, nephridia, and eight sets of dorsoventral pedal retractor muscles. Seriality of organs in supposedly independent molluscan lineages, i.e., in chitons and the deep-sea living fossil monoplacophorans, was assumed to be a relict of ancestral molluscan segmentation and was commonly accepted to support a direct relationship with annelids. We were able to obtain one specimen of a monoplacophoran Antarctic deep-sea species for molecular study. The first molecular data on monoplacophorans, analyzed together with the largest data set of molluscs ever assembled, clearly illustrate that monoplacophorans and chitons form a clade. This ''Serialia'' concept may revolutionize molluscan systematics and may have important implications for metazoan evolution as it allows for new interpretations for primitive segmentation in molluscs.Antarctica ͉ deep sea ͉ Mollusca ͉ Monoplacophora ͉ phylogeny

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“…3 E-H). We could thus identify a band of cilia [representing the so-called ''metatroch'' (43), at the level of ''1'' in Fig. 3 F-H] that demarcates the posterior limit of otx expression from 48 hpf onwards (Fig.…”

Section: An Otx-gbx Morphogenetic Boundary Anteriorly Delimitates Thementioning

confidence: 99%

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

Steinmetz

Zelada-Gonzáles

Burgtorf

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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During frog and fish development, convergent extension movements transform the spherical gastrula into an elongated neurula. Such transformation of a ball-into a worm-shaped embryo is an ancestral and fundamental feature of bilaterian development, yet this is modified or absent in the protostome model organisms Caenorhabditis or Drosophila. In the polychaete annelid Platynereis dumerilii, early embryonic and larval stages resemble a sphere that subsequently elongates into worm shape. Cellular and molecular mechanisms of polychaete body elongation are yet unknown. Our in vivo time-lapse analysis of Platynereis axis elongation reveals that the polychaete neuroectoderm converges and extends by mediolateral cell intercalation. This occurs on both sides of the neural midline, the line of fusion of the slit-like blastopore. Convergent extension moves apart mouth and anus that are both derived from the blastopore. Tissue elongation is actin-dependent but microtubule-independent. Dependence on JNK activity and spatially restricted expression of strabismus indicates involvement of the noncanonical Wnt pathway. We detect a morphogenetic boundary between the converging and extending trunk neuroectoderm and the anterior otx-expressing head neuroectoderm that does not elongate. Our comparative analysis uncovers striking similarities but also differences between convergent extension in the polychaete and in the frog (the classical vertebrate model for convergent extension). Based on these findings, we propose that convergent extension movements of the trunk neuroectoderm represent an ancestral feature of bilaterian development that triggered the separation of mouth and anus along the elongating trunk.amphistomy ͉ axis formation ͉ convergent extension ͉ gastrulation

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Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca

Cited by 136 publications

References 147 publications

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

The morphology and evolutionary significance of the ciliary fields and musculature among marine bryozoan larvae

Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons

Polychaete trunk neuroectoderm converges and extends by mediolateral cell intercalation

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