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Cited by 103Marine Invertebrate Physiology and EcologyNeurobiology and Insect Physiology ResearchDevelopmental Biology and Gene Regulation

Origin and early evolution of neural circuits for the control of ciliary locomotion

Open access
Jékely, Gáspár·2011·Proceedings of the Royal Society B: Biological Sciences
DOI 10.1098/rspb.2010.2027PMC PMC3049052
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Abstract

Behaviour evolved before nervous systems. Various single-celled eukaryotes (protists) and the ciliated larvae of sponges devoid of neurons can display sophisticated behaviours, including phototaxis, gravitaxis or chemotaxis. In single-celled eukaryotes, sensory inputs directly influence the motor behaviour of the cell. In swimming sponge larvae, sensory cells influence the activity of cilia on the same cell, thereby steering the multicellular larva. In these organisms, the efficiency of sensory-to-motor transformation (defined as the ratio of sensory cells to total cell number) is low. With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible. This may have first occurred in a ciliated swimming stage of the first eumetazoans. The first axons may have had en passant synaptic contacts to several ciliated cells to improve the efficiency of sensory-to-motor transformation, thereby allowing a reduction in the number of sensory cells tuned for the same input. This could have allowed the diversification of sensory modalities and of the behavioural repertoire. I propose that the first nervous systems consisted of combined sensory-motor neurons, directly translating sensory input into motor output on locomotor ciliated cells and steering muscle cells. Neuronal circuitry with low levels of integration has been retained in cnidarians and in the ciliated larvae of some marine invertebrates. This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection. The sensory-motor nervous systems of cnidarians and ciliated larvae of diverse phyla show that brains, like all biological structures, are not irreducibly complex.

AI snapshot

Written from the paper’s full text.

TL;DR

This review proposes that the first nervous systems were simple sensory-motor neurons directly controlling ciliary locomotion, with later circuits adding signal amplification and reduced sensory-cell numbers. It argues that low-integration sensory-motor circuits in cnidarians and ciliated larvae provide evidence about early brain evolution.

Key findings

  • The paper proposes that the first neurons were combined sensory-motor neurons that directly translated sensory input into motor output on locomotor ciliated cells and steering muscle cells; such low-integration circuitry has been retained in cnidarians and ciliated larvae of some marine invertebrates.
  • Sensory-to-motor transformation efficiency is estimated as the ratio of sensory structures to total cells controlled: *Chlamydomonas* 1:1; *Volvox rousseletii* about half of 5000 somatic cells have a sufficiently large eyespot (1:2); sponge *Amphimedon queenslandica* larva has a few hundred ciliated photoreceptor cells regulating phototaxis among a few thousand surface cells (about 1:10); *Platynereis* larva uses two directionally shaded photoreceptor neurons to innervate multiciliated cells (1:1000).
  • Synapse-mediated signal amplification is argued to improve sensory-to-motor efficiency by about two orders of magnitude, allowing *Platynereis* to perform phototaxis with only two sensory cells versus hundreds in a similar-sized *Volvox* colony.
  • Spiralian multiciliated ciliary bands concentrate ciliary motors: *Platynereis* has two rows of 12 multiciliated cells, and its apical organ generally contains about 2–4 serotonergic cell bodies, whereas monociliated larvae such as phoronids have many more serotonergic cell bodies (e.g. 30–50 cells in a phoronid larva).

Methods

  • Design: conceptual review and hypothesis paper, not a primary experimental study; it synthesizes comparative behavioural, anatomical, molecular and evo-devo data to outline transition scenarios for early neural circuit evolution.
  • Data or sample: no new sample or dataset; the argument draws on cited organisms including protists, *Volvox*, sponge larvae, cnidarians, *Platynereis*, *Helisoma*, echinoderms, phoronids and other marine larvae.
  • Main analysis: comparative framework using sensory-to-motor transformation ratios and proposed evolutionary transitions, partly based on prior *Platynereis* work and partly on older ideas elaborated with modern data.

Limitations

  • The paper states that knowledge about the early evolution of neural circuits is still fragmentary; traditional terrestrial model organism brains are too large and complex for detailed circuit comparisons, and nematodes may largely misrepresent early brain evolution because their nervous systems are highly evolved and optimized.
  • The paper also notes that the evolutionary origin and ancient versus modern origin of larvae is still debated.
  • Evident from the text: the proposed transition scenarios are hypothetical and partly novel; several claims rely on unpublished results (Conzelmann and Jékely, unpublished), and the comparative phototaxis argument involves independent evolutionary innovations rather than direct ancestral reconstruction.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1098/rspb.2010.2027

Cites

26 of 26 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 111 cited sources checked · 0 supported · 0 flagged

  • Findingnone given
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    Comparison of various phototactic organisms shows that there is no major difference in the efficiency and precision of phototaxis.

    “Comparison of various phototactic organisms shows that there is no major difference in the efficiency and precision of phototaxis.”
    Quote in the paperSubstantial claim
  • Findingreasoning
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    The efficiency of sensory-to-motor transformation, estimated as the ratio of the number of sensory structures to the total number of cells being controlled, is very different between phototactic organisms.

    “What is very different between these organisms is the efficiency of sensory-to-motor transformation, estimated as the ratio of the number of sensory structures to the total number of cells being controlled.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: The costs of building an efficient light-detecting device are similar for all organisms.
  • Interpretationreasoning
    § Abstract

    This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection.

    “This parallel processing stage could have been the starting point for the evolution of more integrated circuits performing the first complex computations such as persistence or coincidence detection.”
    Quote in the paperNot a substantial claim
  • Interpretationnone given
    § Abstract

    In organisms without neurons (protists and sponge larvae), the efficiency of sensory-to-motor transformation, defined as the ratio of sensory cells to total cell number, is low.

    “In these organisms, the efficiency of sensory-to-motor transformation (defined as the ratio of sensory cells to total cell number) is low.”
    Quote in the paperNot a substantial claim
  • Premisenone given
    § 1. Introduction

    Ciliary locomotion, present in single-celled eukaryotes (protists) and also sponge larvae, is the more ancient form of locomotion.

    “Ciliary locomotion, present in single-celled eukaryotes (protists) and also sponge larvae, is the more ancient form of locomotion.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 32
  • Classified as probably not a substantial claim. 32

  • May combine two claims.

    Findingcitation
    § 1. Introduction

    Our studies on the ciliated larvae of Platynereis dumerilii have shown that these larvae have direct sensory-motor neurons and sensory-motor eyes.

    “Our studies on the ciliated larvae of the marine annelid model Platynereis dumerilii have recently shown that these larvae have direct sensory-motor neurons and sensory-motor eyes ([8]; M. Conzelmann and G. Jékely 2010, unpublished).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [8] Jékely,, 2008, Mechanism of phototaxis in marine zooplankton, Nature source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    In the larvae of the annelid Platynereis, two directionally shaded photoreceptor neurons sense light and regulate steering by innervating the multiciliated cells (1:1000 ratio).

    “In the larvae of the annelid Platynereis, two directionally shaded photoreceptor neurons sense light and regulate steering by innervating the multiciliated cells (1 : 1000 ratio, figure 1, and see below).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [8] Jékely,, 2008, Mechanism of phototaxis in marine zooplankton, Nature source

      Not checked in the free run.

  • May combine two claims.

    Findingcitation
    § 4. The evolution of the first neurons to regulate cilia

    Many neuropeptidergic sensory cells directly innervate the ciliary band in Platynereis larvae and the released neuropeptides regulate ciliary beating.

    “Many neuropeptidergic sensory cells also directly innervate the ciliary band in Platynereis larvae and the released neuropeptides regulate ciliary beating (Conzelmann and Jékely, unpublished).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingreasoning
    § 5. The evolution of ciliary bands in protostomes

    The axon of the Platynereis larval eye photoreceptors only forms a few en passant synapses on the adjacent multiciliated cell, but can generate a motor response strong enough to steer the whole larva.

    “For example, the axon of the Platynereis larval eye photoreceptors only forms a few en passant synapses on the adjacent multiciliated cell, but can generate a motor response strong enough to steer the whole larva.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Premisenone given
    § 2. Mechanisms of circuit evolution

    Neuronal circuits evolve by the Darwinian processes of variation and selection.

    “Neuronal circuits evolve by the Darwinian processes of variation and selection.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationnone given
    § 1. Introduction

    The first smooth muscles may have evolved to steer a ciliated organism during tactic behaviours and to contract a sessile adult.

    “The first smooth muscles may have evolved to steer a ciliated organism during tactic behaviours (e.g. photo- or gravitaxis) and to contract a sessile adult.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 1. Introduction

    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]).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Seipel,, 2005, Evolution of striated muscle: jellyfish and the origin of triploblasty, Dev. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § 1. Introduction

    Since sponges represent the deepest branches of the metazoan tree and lack a nervous system, it follows most parsimoniously that the first nervous systems evolved along the stem lineage leading to the eumetazoans.

    “Since sponges represent the deepest branches of the metazoan tree ([3]; but see also [4]) and they lack a nervous system, it follows most parsimoniously that the first nervous systems evolved along the stem lineage leading to the eumetazoans (comprising cnidarians, ctenophores and bilaterians), all possessing a nervous system.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [3] Philippe,, 2009, Phylogenomics revives traditional views on deep animal relationships, Curr. Biol. source

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    • cites [4] Dunn,, 2008, Broad phylogenomic sampling improves resolution of the animal tree of life, Nature source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 1. Introduction

    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].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Seipel,, 2005, Evolution of striated muscle: jellyfish and the origin of triploblasty, Dev. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given
    § Abstract

    With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible.

    “With the advent of neurons, signal amplification and fast, long-range communication between sensory and motor cells became possible.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    An analogous spiral swimming phototactic strategy is found in the multicellular green alga Volvox, and also in the ciliated larvae of animals including sponges, cnidarians, annelids and molluscs.

    “An analogous spiral swimming phototactic strategy is found in the multicellular green alga Volvox [35], and also in the ciliated larvae of animals including sponges [36,37], cnidarians [38,39], annelids [8] and molluscs [40].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [35] Ueki,, 2010, How 5000 independent rowers coordinate their strokes in order to row into the sunlight: phototaxis in the multicellular green alga Volvox, BMC Biol. source

      Not checked in the free run.

    • cites [36] Leys,, 2001, Cytological basis of photoresponsive behavior in a sponge larva, Biol. Bull. source

      Not checked in the free run.

    • cites [37] Maldonado,, 2003, The cellular basis of photobehavior in the tufted parenchymella larva of demosponges, Mar. Biol. source

      Not checked in the free run.

    • cites [8] Jékely,, 2008, Mechanism of phototaxis in marine zooplankton, Nature source

      Not checked in the free run.

  • May combine two claims.

    Premisenone given
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    In the phototactic larvae of the sponge Amphimedon queenslandica, a ring of ciliated photoreceptor cells (a few hundred cells) regulate phototaxis by bending their long, steering cilia, while other surface cells (a few thousand) with shorter cilia contribute to larval locomotion (about 1:10 ratio).

    “In the phototactic larvae of the sponge Amphimedon queenslandica a ring of ciliated photoreceptor cells (a few hundred cells) regulate phototaxis by bending their long, steering cilia. Other cells on the surface of the larva (a few thousand cells) have shorter cilia and contribute to larval locomotion (about 1 : 10 ratio).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisenone given
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    The behavioural repertoire of protists is rather limited, yet the individual behaviours that are present are remarkably sophisticated.

    “The behavioural repertoire of protists is rather limited, yet the individual behaviours that are present are remarkably sophisticated.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 4. The evolution of the first neurons to regulate cilia

    These cells express orthologues of bilaterian neurogenic molecules, indicating that they may represent a protoneuron, an ancestral stage of neuronal cell-type evolution.

    “These cells express orthologues of bilaterian neurogenic molecules, indicating that they may represent a protoneuron, an ancestral stage of neuronal cell-type evolution [41].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [41] Richards,, 2008, Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit, Curr. Biol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    Some animal larvae, such as sponges and some cnidarians, perform phototaxis without a nervous system, while others, including some cnidarians and many bilaterians, perform phototaxis with a nervous system.

    “Some animal larvae, such as sponges [36,37] and some cnidarians [38], perform phototaxis without a nervous system, while others, including some cnidarians [39] and many bilaterians [8,40], perform phototaxis with a nervous system.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [36] Leys,, 2001, Cytological basis of photoresponsive behavior in a sponge larva, Biol. Bull. source

      Not checked in the free run.

    • cites [37] Maldonado,, 2003, The cellular basis of photobehavior in the tufted parenchymella larva of demosponges, Mar. Biol. source

      Not checked in the free run.

    • cites [38] Nordström,, 2003, A simple visual system without neurons in jellyfish larvae, Proc. R. Soc. Lond. B source

      Not checked in the free run.

    • cites [39] Plickert,, 2004, Neuropeptides and photic behavior in Cnidaria, Hydrobiologia

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    In Volvox rousseletii, about half of the 5000 somatic cells have a sufficiently large eyespot to allow light detection, and these cells all contribute to phototactic steering (1:2 ratio).

    “In the multicellular Volvox rousseletii, about half of the 5000 somatic cells have a sufficiently large eyespot to allow light detection. These cells, located in the anterior hemisphere of the alga, all contribute to phototactic steering (1 : 2 ratio; [35]).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [35] Ueki,, 2010, How 5000 independent rowers coordinate their strokes in order to row into the sunlight: phototaxis in the multicellular green alga Volvox, BMC Biol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 2. Mechanisms of circuit evolution

    Similar optimization rules apply to the layout of different cortical areas in mammalian brains.

    “Similar rules apply to the layout of different cortical areas in mammalian brains [16].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] Klyachko,, 2003, Connectivity optimization and the positioning of cortical areas, Proc. Natl Acad. Sci. USA source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 2. Mechanisms of circuit evolution

    The placement of the 11 ganglia in the nematode nervous system minimizes the total wiring length.

    “For example, the placement of the 11 ganglia in the nematode nervous system minimizes the total wiring length [14,15].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [14] Cherniak,, 1994, Component placement optimization in the brain, J. Neurosci. source

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    • cites [15] Cherniak,, 1995, Neural component placement, Trends Neurosci. source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 2. Mechanisms of circuit evolution

    The olfactory system of the morinda fruit specialist Drosophila sechellia has been grossly reorganized during the evolution of the species by the expansion of some olfactory sensilla at the expense of others.

    “For example, the olfactory system of the morinda fruit specialist Drosophila sechellia has been grossly reorganized during the evolution of the species by the expansion of some olfactory sensilla at the expense of others [18].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Dekker,, 2006, Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia, Curr. Biol. source

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  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning
    § 2. Mechanisms of circuit evolution

    These changes are expected to show Darwinian gradualism, progressing by small steps in the elaboration, complexification or simplification of circuits.

    “These changes are expected to show Darwinian gradualism, progressing by small steps in the elaboration, complexification or simplification of circuits.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning
    § 3. The efficiency of sensory-to-motor transformation with and without a nervous system

    With the advent of neurons, a similar cost reduction may have occurred for other senses as well.

    “With the advent of neurons a similar cost reduction may have occurred for other senses as well.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § 2. Mechanisms of circuit evolution

    A gain in conduction speed is sometimes so vital that it drives the evolution of giant axons.

    “A gain in conduction speed is sometimes so vital that it drives the evolution of giant axons [20].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [20] Hartline,, 2007, Rapid conduction and the evolution of giant axons and myelinated fibers, Curr. Biol. source

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  • May combine two claims.

    Interpretationcitation
    § 2. Mechanisms of circuit evolution

    The huge benefits of processing information by neurons and the high metabolic, wiring and signalling costs of nervous systems strongly influence nervous system evolution, and must have done so from the very beginnings of brain evolution.

    “The huge benefits of processing information by neurons on the one hand and the high metabolic, wiring and signalling costs of nervous systems on the other, strongly influence nervous system evolution [10–12], and must have done so from the very beginnings of brain evolution.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [10] Laughlin,, 2003, Communication in neuronal networks, Science source

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    • cites [11] Niven,, 2008, Energy limitation as a selective pressure on the evolution of sensory systems, J. Exp. Biol. source

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    • cites [12] Chittka,, 2009, Are bigger brains better?, Curr. Biol. source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    The earliest neurons may have regulated both cilia and muscles in a ciliary locomotor and steering circuit.

    “It is also possible that the earliest neurons regulated both cilia and muscles in a ciliary locomotor and steering circuit (e.g. for phototaxis).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § 5. The evolution of ciliary bands in protostomes

    The serotonergic nervous system seems to support the idea that spiralian larvae use fewer neurons tuned for the same input and have more senses and more elaborate ciliary locomotory control than monociliated larvae.

    “The serotonergic nervous system seems to support this idea.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning
    § 4. The evolution of the first neurons to regulate cilia

    These ciliary swimming vehicles can turn, speed up or slow down, simply through direct regulation by their sensory-motor neurons.

    “These ciliary swimming vehicles can turn, speed up or slow down, simply through direct regulation by their sensory-motor neurons.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    The two cell types could have remained connected electrically or via a chemical synapse.

    “The two cell types could have remained connected electrically or via a chemical synapse (figure 4).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationreasoning
    § 4. The evolution of the first neurons to regulate cilia

    As these first synapses and axons evolved further, the sensory cells could have spread the amplified stimulus to more effector cells by budding off many en passant synapses in a row at the basal side of the ciliated epithelium.

    “As these first synapses and axons evolved further, the sensory cells could have spread the amplified stimulus to more effector cells by budding off many en passant synapses in a row at the basal side of the ciliated epithelium.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given
    § 5. The evolution of ciliary bands in protostomes

    One driving force underlying the evolution of multiciliated cells could have been the improvement of swimming efficiency.

    “One driving force underlying the evolution of these multiciliated cells could have been the improvement of swimming efficiency.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationreasoning
    § 4. The evolution of the first neurons to regulate cilia

    From a sponge larva-like stage with autonomous epithelial sensory-motor cells, one can envisage a gradual transition into a minimally integrated sensory-motor nervous system controlling ciliary locomotion.

    “From such a sponge larva-like stage with autonomous epithelial sensory-motor cells, one can envisage a gradual transition into a minimally integrated sensory-motor nervous system controlling ciliary locomotion.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation
    § 4. The evolution of the first neurons to regulate cilia

    Such sensory-motor peptidergic neurons can also be found in the ciliated larvae of cnidarians and echinoderms, and probably represent a very ancient neuron type.

    “Such sensory-motor peptidergic neurons can also be found in the ciliated larvae of cnidarians and echinoderms [45], and probably represent a very ancient neuron type (Conzelmann and Jékely, unpublished).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [45] Beer,, 2001, Development of serotonin-like and SALMFamide-like immunoreactivity in the nervous system of the sea urchin Psammechinus miliaris, Biol. Bull. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. The evolution of the first neurons to regulate cilia

    These GPCRs originated by lineage-specific expansion, and many are single-exon genes forming clusters in the genome, reminiscent of lineage-specific putative chemosensory GPCRs in other animal groups.

    “These GPCRs originated by lineage-specific expansion, and many are single-exon genes forming clusters in the genome [1], reminiscent of lineage-specific putative chemosensory GPCRs in other animal groups [43].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [1] Srivastava,, 2010, The Amphimedon queenslandica genome and the evolution of animal complexity, Nature source

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    • cites [43] Raible,, 2006, Opsins and clusters of sensory G-protein-coupled receptors in the sea urchin genome, Dev. Biol. source

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  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning
    § 4. The evolution of the first neurons to regulate cilia

    In a ciliated larva, the first sensory cells may have initially secreted neuropeptides or transmitters to regulate neighbouring ciliated cells, thereby altering swimming speed or direction.

    “In a ciliated larva the first sensory cells may have initially secreted neuropeptides or transmitters to regulate neighbouring ciliated cells, thereby altering swimming speed or direction.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationreasoning
    § 4. The evolution of the first neurons to regulate cilia

    To channel signals more precisely and to increase the efficiency of signal transmission, these sensory cells may have developed basal processes and release sites with close contact to the neighbouring target cells.

    “To channel signals more precisely and to increase the efficiency of signal transmission, these sensory cells may have developed basal processes and release sites with close contact to the neighbouring target cells (figure 2a).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation
    § 4. The evolution of the first neurons to regulate cilia

    Besides light, sponge sensory capacities probably include chemosensation, an important input during larval settlement.

    “Besides light, sponge sensory capacities probably include chemosensation, an important input during larval settlement [42].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [42] Avila,, 2006, Habitat selection by larvae of the symbiotic sponge Haliclona caerulea (Hechtel, 1965) (Demospongiae, Haplosclerida), Symbiosis

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. The evolution of the first neurons to regulate cilia

    The sponge genome contains genes coding for neuropeptide processing enzymes and synaptic vesicle release proteins, but no neuropeptides have been identified.

    “The sponge genome contains genes coding for neuropeptide processing enzymes and synaptic vesicle release proteins, however no neuropeptides have been identified [1].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] Srivastava,, 2010, The Amphimedon queenslandica genome and the evolution of animal complexity, Nature source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § 4. The evolution of the first neurons to regulate cilia

    Serotonin was also described in neurons of cnidarian planula larvae, but there is no evidence that it is involved in ciliary locomotion control.

    “Serotonin was also described in neurons of cnidarian planula larvae, but there is no evidence that it is involved in ciliary locomotion control [51].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [51] McCauley,, 1997, Serotonin plays an early role in the metamorphosis of the hydrozoan Phialidium gregarium, Dev. Biol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation
    § 6. The evolution of circuits for muscle contraction

    The first muscle cells and the first neurons may have a common evolutionary origin from a myoepithelial sensory cell.

    “The first muscle cells and the first neurons may even have a common evolutionary origin from a myoepithelial sensory cell, as suggested by Mackie [23].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Mackie,, 1970, Neuroid conduction and the evolution of conducting tissues, Q. Rev. Biol. source

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  • May combine two claims.

    Premisecitation
    § 4. The evolution of the first neurons to regulate cilia

    In many marine invertebrate larvae, locomotion is based on cilia and follows a spiral trajectory with axial rotation in three dimensions.

    “In many marine invertebrate larvae, locomotion is not based on wheels but on cilia, and does not happen in two dimensions, but follows a spiral trajectory with axial rotation in three dimensions [8,53].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] Jékely,, 2008, Mechanism of phototaxis in marine zooplankton, Nature source

      Not checked in the free run.

    • cites [53] Jennings,, 1901, On the significance of the spiral swimming of organisms, Am. Nat. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationnone given
    § 6. The evolution of circuits for muscle contraction

    A further development in nervous system circuitry could have coincided with the evolution of more elaborate musculature, comprising both the circular and the longitudinal muscles of a radially symmetric animal.

    “A further development in nervous system circuitry could have coincided with the evolution of more elaborate musculature, comprising both the circular and the longitudinal muscles of a radially symmetric animal.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    The synaptic targets of the two cells were reorganized in parallel such that the upstream cell lost its contacts to the muscle fibre to be inhibited, and the downstream cell lost its contact to the muscles to be activated by the circuit.

    “The synaptic targets of the two cells were reorganized in parallel such that the upstream cell lost its contacts to the muscle fibre to be inhibited, and the downstream cell lost its contact to the muscles to be activated by the circuit (figure 4b).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    The upstream cell gradually lost the inhibitory transmitter and kept the excitatory one, while the downstream cell kept the inhibitory transmitter.

    “The upstream cell gradually lost the inhibitory transmitter and kept the excitatory one, while the downstream cell kept the inhibitory transmitter.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 6. The evolution of circuits for muscle contraction

    In these circuits, motoneurons form a network connected by gap junctions, allowing the spread of currents to large motor areas.

    “In these circuits, motoneurons form a network connected by gap junctions, allowing the spread of currents to large motor areas.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Mackie,, 2004, Central neural circuitry in the jellyfish Aglantha: a model ‘simple nervous system, Neurosignals source

      Not checked in the free run.

    • Rests on an assumption: Extant cnidarian neural circuits are representative of an ancestral stage of neural circuit evolution.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning
    § 7. Outlook

    Studies in nematodes may largely misrepresent early brain evolution, given that these animals have a highly evolved and optimized nervous system.

    “Studies in nematodes may also largely misrepresent early brain evolution, given that these animals have a highly evolved and optimized nervous system.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 7. Outlook

    General developmental patterning and maybe large-scale circuitry can be compared between animals as distantly related as protostomes and deuterostomes.

    “Even though general developmental patterning [70,71] and maybe even large-scale circuitry [72] can be compared between animals as distantly related as protostomes and deuterostomes, the size and complexity of traditional terrestrial model organism brains make detailed comparisons of circuits difficult.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [70] Denes,, 2007, Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria, Cell source

      Not checked in the free run.

    • cites [71] Lowe,, 2008, Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii, Phil. Trans. R. Soc. B source

      Not checked in the free run.

    • cites [72] Erclik,, 2008, Conserved role of the vsx genes supports a monophyletic origin for bilaterian visual systems, Curr. Biol. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    Subsequent evolution from this stage could have led to neurons that collected sensory inputs from different sensory cells and established long-range contacts with muscles.

    “From this stage of organization subsequent evolution could have led to neurons that collected sensory inputs from different sensory cells and established long-range contacts with muscles.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    At an intermediate stage the sensory cells may have kept synaptic contacts with the effector cells, but may also have contacted a dedicated motoneuron that provided the dominant input in a feed-forward circuit.

    “At an intermediate stage the sensory cells may have kept synaptic contacts with the effector cells, but may also have contacted a dedicated motoneuron that provided the dominant input in a feed-forward circuit.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    This could have allowed economization on wire length.

    “This could have allowed economization on wire length”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    It was this type of concentrated sensory cell arrangement that became prominent in bilaterians, coinciding with the origin of a centralized brain.

    “It was this type of concentrated sensory cell arrangement that became prominent in bilaterians, coinciding with the origin of a centralized brain.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing), S4 (based).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    A hypothetical network such as this could have functioned normally throughout these evolutionary transitions.

    “A hypothetical network such as this could have functioned normally throughout these evolutionary transitions.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation
    § 6. The evolution of circuits for muscle contraction

    These cells may have evolved into persistence or coincidence detectors to integrate signals over time or from numerous sensory cells.

    “These cells may have evolved into persistence or coincidence detectors to integrate signals over time or from numerous sensory cells [65].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [65] Kashtan,, 2004, Topological generalizations of network motifs, Phy. Rev. E source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    Another possible optimization from a radially symmetric stage with a diffused sensory and motor system is the concentration of some of the sensory cells.

    “Another possible optimization from a radially symmetric stage with a diffused sensory and motor system is the concentration of some of the sensory cells.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationnone given
    § 7. Outlook

    The size and complexity of traditional terrestrial model organism brains make detailed comparisons of circuits difficult.

    “Even though general developmental patterning [70,71] and maybe even large-scale circuitry [72] can be compared between animals as distantly related as protostomes and deuterostomes, the size and complexity of traditional terrestrial model organism brains make detailed comparisons of circuits difficult.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    These sign reversing circuits may have evolved gradually from a ganglion motor cell that first used two transmitters-one inhibitory, one excitatory-and innervated two sets of muscles with different receptors.

    “These circuits may have evolved gradually from a ganglion motor cell that first used two transmitters—one inhibitory, one excitatory—and innervated two sets of muscles with different receptors.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    Once this cell duplicated, the two sister cells could have stayed in synaptic contact.

    “Following this scenario, once this cell duplicated, the two sister cells could have stayed in synaptic contact.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 6. The evolution of circuits for muscle contraction

    In the sea anemone Aiptasia, epithelial sensory cells synapse directly on muscles and also synapse on a ganglion cell that has long-range contacts with the nerve plexus.

    “In the sea anemone Aiptasia, epithelial sensory cells, besides synapsing directly on muscles, also synapse on a ganglion cell that has long-range contacts with the nerve plexus.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [64] Westfall,, 2002, Ultrastructural evidence for two-cell and three-cell neural pathways in the tentacle epidermis of the sea anemone Aiptasia pallida, J. Morphol. source

      Not checked in the free run.

    • Rests on an assumption: Extant cnidarian neural circuits are representative of an ancestral stage of neural circuit evolution.

  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning
    § 6. The evolution of circuits for muscle contraction

    This could have combined cells with the same sensory modalities into minimally integrated circuits.

    “could have combined cells with the same sensory modalities into minimally integrated circuits”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation
    § 6. The evolution of circuits for muscle contraction

    These networks are controlled by fast giant axons, such as in the hydrozoan Aglantha, that receive input from mechanosensory cells.

    “These networks are controlled by fast giant axons, such as in the hydrozoan Aglantha [67], that receive input from mechanosensory cells.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Mackie,, 2004, Central neural circuitry in the jellyfish Aglantha: a model ‘simple nervous system, Neurosignals source

      Not checked in the free run.

    • Rests on an assumption: Extant cnidarian neural circuits are representative of an ancestral stage of neural circuit evolution.
58 of 58

  • The paper relies on this without support.

    We know relatively little about the nervous control of ciliary locomotion.

    “Despite its wide phylogenetic distribution and importance, we know relatively little about the nervous control of ciliary locomotion.”

  • The authors state this as an assumption.

    The costs of building an efficient light-detecting device are similar for all organisms.

    “Assuming that the costs of building an efficient light-detecting device are similar for all organisms, the number of such devices divided by the total number of cells gives an estimate of the cost-efficiency of the behaviour.”

  • The paper relies on this without support.

    Extant cnidarian neural circuits are representative of an ancestral stage of neural circuit evolution.

    “Neural circuits representing such a stage are present in cnidarians.”
3 of 3

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?

  • The evolution of neurons and neural circuits allowed life to overcome the limitations imposed by diffusion-limited communication.

    “The evolution of neurons [247] and neural circuits [248] allowed life to overcome the limitations imposed by diffusion-limited communication [249].”

    From Fundamental constraints to the logic of living systems (2024) · cites this paper as [248]

  • The presence of a nervous system increases the efficiency of ciliary control because a few sensors can control many effectors.

    “It has been proposed that the presence of a nervous system increases the efficiency of the control of cilia as a few sensors can control many effectors [6] (see also [4]).”

    From An option space for early neural evolution (2015) · cites this paper as [6]

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.

  • Defined efficiency ratio runs opposite to claimed improvement

    Minor

    The paper defines efficiency as sensory cells divided by total cells, yet treats the decrease from the non-neural examples' ratios (1 : 1 to about 1 : 10) to the annelid's 1 : 1000 as an improvement. That decrease indicates an improvement in cost-efficiency or cells controlled per sensor, not in the ratio as defined.

1 of 1

Cites

Flagged first, then by citations

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Cited by

Sorted by citations

Authors
Jékely, G.
Affiliations
Max Planck Institute for Developmental Biology (DE)
Corresponding author
Jékely, Gáspár
ORCID
Jékely, Gáspár
Venue
Proceedings of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2010-12-01
Volume
278
Issue
1707
Pages
914-922
ISSN
  • 0080-4649 (ISSN-L)
  • 0962-8452
  • 1471-2954
DOI
10.1098/rspb.2010.2027
PMC
PMC3049052
OpenAlex
W2138642090
Semantic Scholar
30ea6d5518901472967889e8a05e441a0253fd51
Cited by
103
References
26
Citations by year
2026: 7 · 2025: 8 · 2024: 8 · 2023: 5 · 2022: 1 · 2021: 14 · 2020: 4 · 2019: 6 · 2018: 5 · 2017: 11 · 2016: 5 · 2015: 9 · 2014: 6 · 2013: 4 · 2012: 6
FWCI
0.53
Type
journal article
Language
en
Open access
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Proceedings of the Royal Society B Biological Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Max Planck Institute for Plasma Physics (submittedVersion)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
nervous system evolution, ciliary locomotion, neural circuits, sensory-motor transformation, sponge larvae, ciliates, Cnidaria, axons, synaptic connectivity, evolution of behavior, phototaxis, chemotaxis, gravitaxis, locomotion control, signal amplification
MeSH terms
Animals, Cilia, Biological Evolution, Larva, Muscle Contraction, Nerve Net, Polychaeta

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.

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