Evolution of striated muscle: Jellyfish and the origin of triploblasty
Open accessAbstract
The larval and polyp stages of extant Cnidaria are bi-layered with an absence of mesoderm and its differentiation products. This anatomy originally prompted the diploblast classification of the cnidarian phylum. The medusa stage, or jellyfish, however, has a more complex anatomy characterized by a swimming bell with a well-developed striated muscle layer. Based on developmental histology of the hydrozoan medusa this muscle derives from the entocodon, a mesoderm-like third cell layer established at the onset of medusa formation. According to recent molecular studies cnidarian homologs to bilaterian mesoderm and myogenic regulators are expressed in the larval and polyp stages as well as in the entocodon and derived striated muscle. Moreover striated and smooth muscle cells may have evolved directly and independently from non-muscle cells as indicated by phylogenetic analysis of myosin heavy chain genes (MHC class II). To accommodate all evidences we propose that striated muscle-based locomotion coevolved with the nervous and digestive systems in a basic metazoan Bauplan from which the ancestors of the Ctenophora (comb jellyfish), Cnidaria (jellyfish and polyps), as well as the Bilateria are derived. We argue for a motile tri-layered cnidarian ancestor and a monophyletic descent of striated muscle in Cnidaria and Bilateria. As a consequence, diploblasty evolved secondarily in cnidarian larvae and polyps.
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- Findingcitation
Mitochondrial DNA structure does not strictly correlate with phylogeny.
“There is, however, no strict correlation of mtDNA structure with phylogeny.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Nosek et al., 1998 source
Not checked in the free run.
- Interpretationreasoning
All the basic anatomical elements probably co-evolved as integrated functional units in the basic Bauplan.
“All the basic anatomical elements probably co-evolved as integrated functional units in the basic Bauplan.”
Quote in the paperNot a substantial claim - Premisecitation
In Leptomedusa and a few Anthomedusa, striated muscle is completely covered by flagellated smooth muscle epithelia.
“In the Leptomedusa(Chapman, 1968) and few Anthomedusa(Hyman, 1940) the striated muscle (red) is completely covered (A, A1) by flagellated smooth muscle epithelia (green)”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Chapman, 1968 source
Not checked in the free run.
- cites Hyman, 1940
Not checked in the free run.
- Interpretationreasoning
The available data suggest that striated muscle originated very early.
“Together these data suggest a very early origin of the striated muscle.”
Quote in the paperSubstantial claim - Premisecitation
All striated and smooth muscles and RFamide-positive nerve cells of the subumbrella come from the outer layer of the entocodon.
“All of the striated and smooth muscles and the RFamidepositive nerve cells of the subumbrella derive from the outer layer of the entocodon”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Seipel et al., 2004a
Not checked in the free run.
- cites Tardent, 1978
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- Interpretationreasoning
The developmental histology and bell anatomy of Medusozoa show that much cnidarian anatomy and development cannot be explained by diploblasty.
“In summary, the developmental histology and the anatomy of the bell of the Medusozoa demonstrates that much of cnidarian anatomy and development cannot be sufficiently explained by diploblasty.”
Quote in the paperSubstantial claim - Interpretationreasoning
Conservation of molecular control mechanisms in mesoderm and myogenic patterning across triploblast phyla indicates that early muscle evolution passed a selective bottleneck.
“Furthermore the extent of conservation of the molecular control mechanisms in mesoderm and myogenic patterning throughout the triploblast phyla indicates that early muscle evolution passed a selective bottleneck.”
Quote in the paperSubstantial claim - Interpretationcitation
The entocodon qualifies as a third germ layer because its cells are separated from ectoderm and endoderm by an extracellular matrix.
“Because the entocodon cells are clearly separated from the ectoderm and endoderm by the formation of an extracellular matrix (Bo ¨lsterli, 1977) the entocodon qualifies per definition as a third germ layer”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Boero et al., 1998 source
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- cites Nielsen, 1995
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- Premisecitation
Ctenophora may be triploblastic according to cell lineage analysis and anatomy.
“Moreover, Ctenophora are potentially triploblastic according to cell lineage analysis (Martindale and Henry, 1999) and anatomy (Hernandez-Nicaise and Franc, 1993).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Martindale and Henry, 1999 source
Not checked in the free run.
- cites Hernandez-Nicaise and Franc, 1993
Not checked in the free run.
- Interpretationown data
Certain bilaterian myogenic gene cognates are recruited in medusa development to differentiate muscle and non-muscle tissues.
“Together these data indicate that cognates of certain bilaterian myogenic genes are recruited to differentiate muscle and non-muscle tissues in medusa development.”
Quote in the paperSubstantial claim - Interpretationreasoning
Diploblasty arose secondarily in cnidarian larvae and polyps.
“As a consequence, diploblasty evolved secondarily in cnidarian larvae and polyps.”
Quote in the paperSubstantial claim - Interpretationreasoning
The most parsimonious hypothesis, considering recent molecular, cellular, and developmental data, is that a motile life form with mesodermate-like development was the common ancestor of Ctenophora, Cnidaria, and Bilateria.
“In summary it appears that the most parsimonious hypothesis taking into account the recent molecular, cellular, and developmental data is based on a motile life form with mesodermate-like development as a common ancestor of Ctenophora, Cnidaria, and Bilateria.”
Quote in the paperSubstantial claim- Rests on an assumption: Motile-to-sessile transitions have happened many times among aquatic invertebrates, and in some filter feeders this change came with reduced neuromuscular complexity.
- Rests on an assumption: Ctenophora have no permanent sessile stages.
- Rests on an assumption: Ctenophora possess mesodermate-like development and histology.
- Premisecitation
The polyp and medusa stages can be reduced or completely absent in Hydrozoa and Scyphozoa.
“The polyp stage as well as the medusa stage can be reduced or completely absent in Hydrozoa and Scyphozoa (Boero and Bouillon, 1987;Bouillon and Boero, 2000;Piraino et al., 2004;Tardent, 1978).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Boero and Bouillon, 1987
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- cites Bouillon and Boero, 2000
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- cites Piraino et al., 2004 source
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- Premisenone given
There is no evidence that a diploblastic phase was preserved during the blastula-gastrula transition in any bilaterian embryo.
“Furthermore it is remarkable that there is no evidence for the preservation of a diploblastic phase during the blastulagastrula transition in any bilaterian embryo.”
Quote in the paperNot a substantial claim - Premisecitation
Striated and smooth muscle cells may have arisen directly and separately from non-muscle cells, as indicated by phylogenetic analysis of MHC class II genes.
“Moreover striated and smooth muscle cells may have evolved directly and independently from non-muscle cells as indicated by phylogenetic analysis of myosin heavy chain genes (MHC class II).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Goodson and Spudich, 1993
Not checked in the free run.
- Premisenone given
Among extant phyla, diploblasty is documented only for the cnidarian larva and the sessile polyp stage.
“Within the anatomies of the extant phyla, however, diploblasty is properly documented only for the cnidarian larva and the sessile polyp stage.”
Quote in the paperSubstantial claim - Premisecitation
Two strains of the same species can have circular or linear mitochondrial DNA.
“This is carried to an extreme where two strains of the same species have circular or linear mtDNA, respectively (reviewed in Nosek et al., 1998).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Nosek et al., 1998 source
Not checked in the free run.
- Premisecitation
According to rRNA phylogeny, Ctenophora is basal to Cnidaria.
“according to rRNA phylogeny this phylum is positioned basal to the Cnidaria (Fig. 1B; Ball et al., 2004;Cavalier-Smith and Chao, 2003;Collins and Valentine, 2001;Halanych, 2004;Medina et al., 2001;Podar et al., 2001).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Ball et al., 2004 source
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- cites Cavalier-Smith and Chao, 2003
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- cites Collins and Valentine, 2001
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- Premisecitation
In hydrozoan medusae, striated muscle develops from the entocodon, a mesoderm-like third cell layer formed when medusa development begins.
“Based on developmental histology of the hydrozoan medusa this muscle derives from the entocodon, a mesoderm-like third cell layer established at the onset of medusa formation.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Seipel et al., 2004a
Not checked in the free run.
- cites Tardent, 1978
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- Premisecitation
In Scyphomedusae and Cubomedusae, striated muscle is covered by a non-muscled epithelium.
“while in the Scyphomedusa and Cubomedusae the striated muscle is covered by a non-muscled epithelium(Chapman, 1999;Franc, 1993).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Chapman, 1999 source
Not checked in the free run.
- cites Franc, 1993
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- Interpretationcitation
Radial symmetry may be a secondary trait superimposed on a basically bilateral body plan.
“In fact the radial symmetry may be a secondary trait superimposed on a basically bilateral body plan (Ball et al., 2004), a situation similar to the pentamery of the adult echinoderms.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Ball et al., 2004 source
Not checked in the free run.
- Interpretationnone given
The evolution of anatomical elements capable of rapid locomotion required the simultaneous emergence of a digestive support system and a concurrent connection between musculature and nervous system.
“The evolution of anatomical elements able to generate rapid locomotion required the simultaneous emergence of a digestive support system and a concurrent connection of musculature and nervous system.”
Quote in the paperNot a substantial claim - Interpretationreasoning
Molecular evidence supports a close evolutionary link between muscle and nerve cells and their origin from a common myoepithelial precursor.
“The molecular evidence supports the hypothesis that muscle and nerve cells are closely linked in evolution and derive from a common myoepithelial precursor.”
Quote in the paperSubstantial claim - Interpretationreasoning
It is plausible that the same genes are used to differentiate both larval and medusa cell types.
“Hence it is plausible that the same genes are used in the differentiation of both larval and medusa cell types.”
Quote in the paperSubstantial claim - Interpretationreasoning
The medusa is the only cnidarian life stage that forms bilaterian-like striated muscle.
“The only cnidarian life stage that differentiates bilaterian-like striated muscle is the medusa.”
Quote in the paperSubstantial claim - Premisecitation
Complete loss of the medusa has frequently occurred in several hydrozoan families.
“A complete loss of the medusa has frequently occurred in several hydrozoan families (Boero et al., 1992)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Boero et al., 1992
Not checked in the free run.
- Interpretationreasoning
Cnidaria derive from a motile pre-zootype metazoan with mesodermate and possibly bilaterian anatomical elements.
“In summary it appears that Cnidaria derive from a motile pre-zootype metazoan featuring mesodermate and possibly bilaterian elements of anatomy.”
Quote in the paperSubstantial claim - Premisecitation
In many Anthomedusa, striated muscle is only partially covered by flagellated smooth muscle over the radial canals.
“In many Anthomedusa(Bouillon, 1993) the striated muscle is only partially covered (A2) by flagellated smooth muscle over the radial canals.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Bouillon, 1993
Not checked in the free run.
- Premisecitation
Cnidarian homologs of bilaterian mesoderm and myogenic regulators are expressed in larval and polyp stages and in the entocodon and its derived striated muscle.
“According to recent molecular studies cnidarian homologs to bilaterian mesoderm and myogenic regulators are expressed in the larval and polyp stages as well as in the entocodon and derived striated muscle.”
Quote in the paperSubstantial claim0 of 2 sources checked - Interpretationreasoning
Striated muscle probably did not arise from smooth muscle myoepithelia of planula or polyp ancestors but evolved directly from non-muscle cells.
“Moreover, it appears unlikely that striated muscle derived from smooth muscle myoepithelia of a potential planula or polyp ancestors, but rather evolved directly from non-muscle cells.”
Quote in the paperSubstantial claim - Interpretationreasoning
Molecular developmental analysis of hydrozoan jellyfish and motor protein evolution support a metazoan phylogeny with a nonsessile, tri-layered, possibly medusa-like ancestor at the cnidarian base.
“The molecular developmental analysis of the hydrozoan jellyfish and the evolutionary relationship of motor proteins like myosin support a metazoan phylogeny with a nonsessile, tri-layered, possibly medusa-like ancestor at the cnidarian base.”
Quote in the paperSubstantial claim - Interpretationreasoning
In this scenario, the evolution of the basic Bauplan did not include a diploblast stage.
“In this scenario the evolution of the basic Bauplan did not include a diploblast stage.”
Quote in the paperSubstantial claim - Interpretationreasoning
A sessile cnidarian ancestor is hard to reconcile with the fact that the sessile lifestyle was abandoned only in the Medusozoa ancestor while it shared habitats with Anthozoa.
“If there was a sessile cnidarian ancestor it is difficult to understand why this highly successful life style was abandoned only in the ancestor of the Medusozoa while sharing the same habitats with that of the Anthozoa.”
Quote in the paperSubstantial claim - Premisecitation
A temperature shift may be enough to switch from medusa budding to polyp budding.
“a temperature shift may suffice to change from medusa budding to polyp budding (Werner, 1963).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Werner, 1963 source
Not checked in the free run.
- Interpretationreasoning
Striated muscle-based locomotion coevolved with nervous and digestive systems in a basic metazoan Bauplan ancestral to Ctenophora, Cnidaria, and Bilateria.
“To accommodate all evidences we propose that striated muscle-based locomotion coevolved with the nervous and digestive systems in a basic metazoan Bauplan from which the ancestors of the Ctenophora (comb jellyfish), Cnidaria (jellyfish and polyps), as well as the Bilateria are derived.”
Quote in the paperSubstantial claim
- May combine two claims. 7
- Classified as probably not a substantial claim. 4
May combine two claims.
InterpretationreasoningA triploblast jellyfish ancestor is supported by entocodon-derived striated muscle and by similarity of jellyfish myogenic regulators to bilaterian mesoderm and myogenic factors.
“Two observations corroborate the existence of a triploblast jellyfish ancestor: (1) jellyfish striated muscle develops from a mesoderm-like layer (entocodon), and (2) jellyfish myogenesis is controlled by regulators similar to bilaterian mesoderm and myogenic factors.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S2 (checkable), S4 (based).
Interpretationnone givenAssuming evolutionary principles have not changed since the first animals, replacing ciliary motility with muscle-driven locomotion must have been an important selective advantage for prey capture and escape.
“Under the assumption that the principles of evolution have not changed since the first animals appeared, the replacement of ciliary motility by muscle-driven locomotion must have represented an important selective advantage in preying and escape.”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The principles of evolution have not changed since the first animals appeared.
May combine two claims.
InterpretationreasoningThe linearization of mitochondrial DNA in Medusozoa likely had little selective value and happened early, after the split from Anthozoa and/or Bilateria.
“Thus the linearization of the mtDNA in the Medusozoa was likely of little selective value and occurred early, after the separation from the Anthozoa and/or Bilateria.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningThe cnidarian ancestor was motile and tri-layered, and striated muscle descended monophyletically in Cnidaria and Bilateria.
“We argue for a motile tri-layered cnidarian ancestor and a monophyletic descent of striated muscle in Cnidaria and Bilateria.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing).
PremisecitationUnder the polyp-first hypothesis, a simpler polyp form would give rise to a more complex medusa while the polyp continued to exist alongside it in the life cycle.
“according to Hyman (1940) the polyp first hypothesis would present ''the curious spectacle of a lower type (polyp) evolving into a higher type (medusa) and continuing to exist simultaneously as part of its life cycle''.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hyman (1940)
Not checked in the free run.
Probably not a substantial claim: may not pass S2 (checkable), S4 (based).
Interpretationnone givenThere were placement constraints on the basic anatomical elements within the body and relative to each other.
“Additionally there were placement constraints for the basic anatomical elements within the body and with respect to each other.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationcitationThe term diploblast is questionable for an animal phylum and applies only to the anatomy of the cnidarian larva and polyp.
“Indeed, the term diploblast becomes questionable with respect to an animal phylum (Ball et al., 2004;Hyman, 1940;Willmer, 1990), as it is appropriate only for the anatomy of the cnidarian larva and polyp.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Ball et al., 2004
Not checked in the free run.
- cites Hyman, 1940
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- cites Willmer, 1990
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May combine two claims.
PremisecitationVarious unrelated groups-plants, fungi, slime molds, yeast, and ciliates-carry linear mitochondrial DNA, with the trait appearing in scattered positions across phylogenies.
“Linear mtDNA is known to occur in plants, fungi, slime molds, yeast, or ciliates, often randomly scattered in the phylogenies.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Nosek et al., 1998
Not checked in the free run.
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationnone givenLinear mitochondrial DNA in Medusozoa is more derived than the circular mitochondrial DNA of Anthozoa and Bilateria.
“Compared to the circular mtDNA of the anthozoans and bilaterians, linear mtDNA appears to be more derived.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationLarval and polyp stages of living Cnidaria consist of two cell layers and lack mesoderm and its differentiated products.
“The larval and polyp stages of extant Cnidaria are bi-layered with an absence of mesoderm and its differentiation products.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Bouillon, 1993
Not checked in the free run.
- cites Hyman, 1940
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- cites Tardent, 1978
Not checked in the free run.
May combine two claims.
PremisecitationThe medusa stage has a complex anatomy with a swimming bell and a well-developed striated muscle layer.
“The medusa stage, or jellyfish, however, has a more complex anatomy characterized by a swimming bell with a well-developed striated muscle layer.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Bölsterli, 1977
Not checked in the free run.
- cites Gröger et al., 1999 source
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- cites Schuchert et al., 1993
Not checked in the free run.
The authors state this as an assumption.
Ancestral genomes are sufficiently conserved in living cnidarians to study developmental regulators and their differentiation products for evolutionary research.
“Since cnidarian anatomy appears to have little changed since Precambrian times it can be assumed that the ancestral genomes are suitably well conserved in the extant cnidarian species to investigate developmental regulators and their differentiation products for evolutionary studies.”
The authors state this as an assumption.
The principles of evolution have not changed since the first animals appeared.
“Under the assumption that the principles of evolution have not changed since the first animals appeared”
The authors state this as an assumption.
The model is based on a parenchymula- or phagocytella-like ancestor.
“Its cellular organization is highly speculative but according to the presented data we have based the model on a parenchymula or phagocytellalike ancestor (Grell et al., 1980).”
The paper relies on this without support.
Motile-to-sessile transitions have happened many times among aquatic invertebrates, and in some filter feeders this change came with reduced neuromuscular complexity.
“Furthermore the transition from a motile to a sessile life style is not exclusive to cnidarians but evidently has occurred repeatedly in various aquatic invertebrates, sometimes accompanied by reduction in neuromuscular complexity, as observed in the filter feeders.”
The paper relies on this without support.
Ctenophora have no permanent sessile stages.
“There are no permanent sessile stages in this phylum”
The paper relies on this without support.
Ctenophora possess mesodermate-like development and histology.
“they have a mesodermate-like development and histology”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pan-eumetazoan conservation of striated and smooth muscle includes conserved cellular morphology, function, regulatory state (myogenic bHLH factors and MEF2), and downstream effector genes (e.g., myosin heavy chain).
“Here the distinctive cellular morphology, the function, and underlying these, the regulatory state consisting of myogenic bHLH factors and MEF2, plus downstream effector genes exemplified by the myosin heavy chain contractile protein are all conserved (Seipel and Schmid, 2005).”
From Evolution of Gene Regulatory Networks Controlling Body Plan Development (2011) · cites this paper as Seipel and Schmid, 2005
The sections “The evolution of striated and smooth muscle” and “Mesoderm and myogenic regulatory genes” describe similar vertebrate and medusa striated-muscle ultrastructure, related myosin heavy chains, and myogenic regulatory genes. Table 1 also lists bHLH factors and MEF2 across eumetazoan groups. These passages do not establish that the full combination of morphology, function, regulatory state, and effector genes is conserved in both striated and smooth muscle throughout Eumetazoa. Page numbers were not available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe eumetazoan genes of ancient eukaryotic ancestry descended from approximately 5,148 eukaryotic progenitors by nearly one thousand gene duplications along the eumetazoan stem, after early radiation of eukaryotes about 1100-1500 Mya but prior to divergence of cnidarians and bilaterians.
“The eumetazoan genes of ancient eukaryotic ancestry are themselves descended from approximately ~5,148 eukaryotic progenitors by nearly one thousand gene duplications along the eumetazoan stem, that is, after the early radiation of eukaryotes ~1100-1500 Mya (60) but prior to the divergence of cnidarians and bilaterians (32).”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [60]
Complex muscle-based locomotory circuits may have evolved independently in cnidarians and bilaterians.
“Given the very different mechanics of muscle-based locomotion in cnidarians (polyp and medusa forms) and in bilaterians (worm-like body), complex muscle-based locomotory circuits may have evolved independently in the two groups (for a detailed discussion of the ancestral form of locomotion in cnidarians and the origin of striated muscles, see [9]).”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [9]
Muscle-based motor systems are very ancient and trace back to the stem eumetazoan.
“Muscle-based motor systems are also very ancient and trace back to the stem eumetazoan [9].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [9]
Muscle-based motor systems evolved very early and were probably already present in the stem eumetazoan lineage.
“Muscle-based motor systems also evolved very early, and were probably already present in the stem eumetazoan lineage [9].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [9]
Certain differentiation gene batteries composed of orthologous effector genes and the regulatory state drivers that activate them are known in all bilaterian animals investigated and even in cnidarians, e.g., in muscle cells, neurons, photoreceptor cells, and neurosecretory cells.
“Certain differentiation gene batteries composed of orthologous effector genes and the regulatory state drivers that activate them are known in all bilaterian animals investigated and even in cnidarians, e.g., in muscle cells (5) neurons (13), photoreceptor cells (14 -17), and neurosecretory cells (17).”
From Transphyletic conservation of developmental regulatory state in animal evolution (2011) · cites this paper as [5]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Cambrian age conflicts with a cited fossil report
MinorThe text cites Hagadorn et al. (2002) for fossils from mid-Cambrian strata, but the paper's reference list identifies that report as describing a late Cambrian shoreline.
“large scyphozoan-like medusae and ctenophores are reported from mid-Cambrian strata (Chen and Zhou, 1997;Hagadorn et al., 2002).”
“Hagadorn, J.W., Dott, R.H., Damrow, D., 2002. Stranded on a late Cambrian shoreline: medusae from central Wisconsin.”
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- Authors
- Seipel, K., & Schmid, V.
- Affiliations
- University of Basel (CH)
- Corresponding author
- Schmid, Volker
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2005-06
- Volume
- 282
- Issue
- 1
- Pages
- 14-26
- ISSN
- 0012-1606 (ISSN-L)
- OpenAlex
- W2009856397
- Cited by
- 172
- References
- 138
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 6 · 2023: 5 · 2022: 9 · 2021: 2 · 2020: 6 · 2019: 7 · 2018: 8 · 2017: 7 · 2016: 6 · 2015: 13 · 2014: 5 · 2013: 7 · 2012: 9
- FWCI
- 15.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2968 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Yale University
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- Cnidaria, jellyfish, Medusa, mesoderm, Ctenophora, bilaterian origin, locomotion, nervous system evolution, digestive system evolution
- MeSH terms
- Animals, Cell Differentiation, Cnidaria, Biological Evolution, Genes, Regulator, Germ Layers, Larva, Life Cycle Stages, Mesoderm, Models, Biological, Muscle, Skeletal, Gene Expression Regulation, Developmental, Myosin Heavy Chains
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