Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current

Thompson, Ammon; Infield, Daniel T.; Smith, Adam R.; Smith, G. Troy; Ahern, Christopher A.; Zakon, Harold H.

doi:10.1371/journal.pbio.2004892

Cited by 16 publications

(11 citation statements)

References 64 publications

(83 reference statements)

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“…Brains of related species consist mainly of homologous neurons-neurons that share the same developmental origin-and behavior evolution may result from changes in the connectivity or physiology of homologous neurons [2]. Several studies have begun to elucidate how changes in homologous neurons have contributed to behavioral evolution [3][4][5][6][7][8][9][10][11][12]. But a satisfying answer to the broad evolutionary questions posed above requires a systematic methodology to identify and functionally manipulate homologous neurons.…”

Section: Introductionmentioning

confidence: 99%

Neural Evolution of Context-Dependent Fly Song

et al. 2019

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Section: Introductionmentioning

confidence: 99%

Neural Evolution of Context-Dependent Fly Song

et al. 2019

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“…These include genes for steroid receptors and enzymes in steroidogenic pathways, as well as various ion channels that likely control the continuous firing frequency of PN neurons. Thompson et al (2018) , identified a novel voltage-gated Na+ channel ( scn4ab1 ) expressed in the EMNs that resulted from a gene duplication within apteronotids. This channel has amino acid substitutions that prevent it from closing completely.…”

Section: Contributions Of Molecular Studies To the Neuroethology Of Social Behaviormentioning

confidence: 99%

Vocal and Electric Fish: Revisiting a Comparison of Two Teleost Models in the Neuroethology of Social Behavior

Dunlap

Koukos

Chagnaud

et al. 2021

Front. Neural Circuits

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The communication behaviors of vocal fish and electric fish are among the vertebrate social behaviors best understood at the level of neural circuits. Both forms of signaling rely on midbrain inputs to hindbrain pattern generators that activate peripheral effectors (sonic muscles and electrocytes) to produce pulsatile signals that are modulated by frequency/repetition rate, amplitude and call duration. To generate signals that vary by sex, male phenotype, and social context, these circuits are responsive to a wide range of hormones and neuromodulators acting on different timescales at multiple loci. Bass and Zakon (2005) reviewed the behavioral neuroendocrinology of these two teleost groups, comparing how the regulation of their communication systems have both converged and diverged during their parallel evolution. Here, we revisit this comparison and review the complementary developments over the past 16 years. We (a) summarize recent work that expands our knowledge of the neural circuits underlying these two communication systems, (b) review parallel studies on the action of neuromodulators (e.g., serotonin, AVT, melatonin), brain steroidogenesis (via aromatase), and social stimuli on the output of these circuits, (c) highlight recent transcriptomic studies that illustrate how contemporary molecular methods have elucidated the genetic regulation of social behavior in these fish, and (d) describe recent studies of mochokid catfish, which use both vocal and electric communication, and that use both vocal and electric communication and consider how these two systems are spliced together in the same species. Finally, we offer avenues for future research to further probe how similarities and differences between these two communication systems emerge over ontogeny and evolution.

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“…A striking example of the independent evolution of persistent sodium currents is in the specialized Na v 1.4 channel isoforms for the muscle-derived electric organs of weakly-electric fish, which can generate electrical pulses in excesses of 1 kHz for sensing their nocturnal environment and the electro-communication with other fish ( Thompson et al, 2018 ). The electromotor neurons of weakly-electric fish can fire at a faster rate of any known animal neuron, using a persistent sodium current generated from the modification of its structural elements for inactivation (S4-S5 linker of Domain IV) of their Na v 1.4 channels ( Thompson et al, 2018 ).…”

Section: “Persistent” Sodium Currents Are Common In Different Invertementioning

confidence: 99%

Eukaryotic Voltage-Gated Sodium Channels: On Their Origins, Asymmetries, Losses, Diversification and Adaptations

et al. 2018

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The appearance of voltage-gated, sodium-selective channels with rapid gating kinetics was a limiting factor in the evolution of nervous systems. Two rounds of domain duplications generated a common 24 transmembrane segment (4 × 6 TM) template that is shared amongst voltage-gated sodium (Nav1 and Nav2) and calcium channels (Cav1, Cav2, and Cav3) and leak channel (NALCN) plus homologs from yeast, different single-cell protists (heterokont and unikont) and algae (green and brown). A shared architecture in 4 × 6 TM channels include an asymmetrical arrangement of extended extracellular L5/L6 turrets containing a 4-0-2-2 pattern of cysteines, glycosylated residues, a universally short III-IV cytoplasmic linker and often a recognizable, C-terminal PDZ binding motif. Six intron splice junctions are conserved in the first domain, including a rare U12-type of the minor spliceosome provides support for a shared heritage for sodium and calcium channels, and a separate lineage for NALCN. The asymmetrically arranged pores of 4x6 TM channels allows for a changeable ion selectivity by means of a single lysine residue change in the high field strength site of the ion selectivity filter in Domains II or III. Multicellularity and the appearance of systems was an impetus for Nav1 channels to adapt to sodium ion selectivity and fast ion gating. A non-selective, and slowly gating Nav2 channel homolog in single cell eukaryotes, predate the diversification of Nav1 channels from a basal homolog in a common ancestor to extant cnidarians to the nine vertebrate Nav1.x channel genes plus Nax. A close kinship between Nav2 and Nav1 homologs is evident in the sharing of most (twenty) intron splice junctions. Different metazoan groups have lost their Nav1 channel genes altogether, while vertebrates rapidly expanded their gene numbers. The expansion in vertebrate Nav1 channel genes fills unique functional niches and generates overlapping properties contributing to redundancies. Specific nervous system adaptations include cytoplasmic linkers with phosphorylation sites and tethered elements to protein assemblies in First Initial Segments and nodes of Ranvier. Analogous accessory beta subunit appeared alongside Nav1 channels within different animal sub-phyla. Nav1 channels contribute to pace-making as persistent or resurgent currents, the former which is widespread across animals, while the latter is a likely vertebrate adaptation.

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Rapid evolution of a voltage-gated sodium channel gene in a lineage of electric fish leads to a persistent sodium current

Cited by 16 publications

References 64 publications

Neural Evolution of Context-Dependent Fly Song

Neural Evolution of Context-Dependent Fly Song

Vocal and Electric Fish: Revisiting a Comparison of Two Teleost Models in the Neuroethology of Social Behavior

Eukaryotic Voltage-Gated Sodium Channels: On Their Origins, Asymmetries, Losses, Diversification and Adaptations

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