Ontogeny and evolution of electric organs in gymnotiform fish

Kirschbaum, Frank; Schwassmann, Horst O.

doi:10.1016/j.jphysparis.2008.10.008

Cited by 28 publications

(29 citation statements)

References 11 publications

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“…Larval EOs that precede the adult EO are present in both Mormyrid and Gymnotiform species (Franchina, 1997;Kirschbaum and Schwassmann, 2008). The neurogenic organs of Apteronotids arise after the development and loss of a myogenic larval organ (Kirschbaum, 1983).…”

Section: The Structure and Function Of Gymnotiform And Mormyrid Electmentioning

confidence: 99%

Electrocyte physiology: 50 years later

Markham

2013

Journal of Experimental Biology

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SummaryWeakly electric gymnotiform and mormyrid fish generate and detect weak electric fields to image their worlds and communicate. These multi-purpose electric signals are generated by electrocytes, the specialized electric organ (EO) cells that produce the electric organ discharge (EOD). Just over 50years ago the first experimental analyses of electrocyte physiology demonstrated that the EOD is produced and shaped by the timing and waveform of electrocyte action potentials (APs). Electrocytes of some species generate a single AP from a distinct region of excitable membrane, and this AP waveform determines EOD waveform. In other species, electrocytes possess two independent regions of excitable membrane that generate asynchronous APs with different waveforms, thereby increasing EOD complexity. Signal complexity is further enhanced in some gymnotiforms by the spatio-temporal activation of distinct EO regions with different electrocyte properties. For many mormyrids, additional EOD waveform components are produced by APs that propagate along stalks that connect postsynaptic regions to the main body of the electrocyte. I review here the history of research on electrocyte physiology in weakly electric fish, as well as recent discoveries of key phenomena not anticipated during early work in this field. Recent areas of investigation include the regulation of electrocyte activity by steroid and peptide hormones, the molecular evolution of electrocyte ion channels, and the evolutionary selection of ion channels expressed in excitable cells. These emerging research areas have generated renewed interest in electrocyte function and clear future directions for research addressing a broad range of new and important questions.

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Section: The Structure and Function Of Gymnotiform And Mormyrid Electmentioning

confidence: 99%

Electrocyte physiology: 50 years later

Markham

2013

Journal of Experimental Biology

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“…Testing whether changes in Scn4aa expression coincided with two independent origins of adult EO myo requires a robust phylogeny on which to infer the timing of these events. Although a sound knowledge of mormyroid phylogeny has been acquired using genetic data (9,22,27,28), the overall gymnotiform phylogeny has remained less resolved (14,19,29,30). Thus, we inferred phylogenetic relationships among the teleosts that we investigated using four datasets: all nucleotide positions of both paralogs concatenated ("Concat"), all positions of each gene separately, and only third-codon positions of the concatenated data set ("Concat3rd").…”

Section: Changes In Paralog Expression In Electric Fish Relative To Omentioning

confidence: 99%

Old gene duplication facilitates origin and diversification of an innovative communication system—twice

Arnegard

Zwickl

et al. 2010

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

117

119

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The genetic basis of parallel innovation remains poorly understood due to the rarity of independent origins of the same complex trait among model organisms. We focus on two groups of teleost fishes that independently gained myogenic electric organs underlying electrical communication. Earlier work suggested that a voltagegated sodium channel gene (Scn4aa), which arose by whole-genome duplication, was neofunctionalized for expression in electric organ and subsequently experienced strong positive selection. However, it was not possible to determine if these changes were temporally linked to the independent origins of myogenic electric organs in both lineages. Here, we test predictions of such a relationship. We show that Scn4aa co-option and rapid sequence evolution were tightly coupled to the two origins of electric organ, providing strong evidence that Scn4aa contributed to parallel innovations underlying the evolutionary diversification of each electric fish group. Independent evolution of electric organs and Scn4aa co-option occurred more than 100 million years following the origin of Scn4aa by duplication. During subsequent diversification of the electrical communication channels, amino acid substitutions in both groups occurred in the same regions of the sodium channel that likely contribute to electric signal variation. Thus, the phenotypic similarities between independent electric fish groups are also associated with striking parallelism at genetic and molecular levels. Our results show that gene duplication can contribute to remarkably similar innovations in repeatable ways even after long waiting periods between gene duplication and the origins of novelty.evolutionary novelty | ion channel | independent species radiations | gymnotiforms | mormyroids T he evolution of novelty is a key process in the diversification of life, yet investigating genetic changes associated with novelty remains one of evolutionary biology's greatest challenges (1, 2). Regressive losses of complex traits have received much attention (3, 4), yet such cases offer limited insights into the constructive evolution of complex novel traits. It has long been suspected that gene duplication is an important source of genetic raw material for evolutionary novelty (5). However, the innovations that have been linked to gene duplication are typically simple phenotypes, such as the modification of protein function (6) rather than the de novo construction of a complex trait (7). Comparing relationships between a single gene duplicate and multiple independent gains of the same complex trait has not been possible previously in any system. Here, we test whether a duplicated voltage-gated Na + channel gene directly contributed to independently derived organs of electrical communication in teleost fishes.Although distantly related, African mormyroid and South American gymnotiform fishes independently gained myogenic electric organs, which produce electrical communication signals in both groups (Fig. S1). This novel organ is a key innovation in commu...

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“…Of these, approximately 173 species are gymnotiforms, or South American knifefishes, and in all but one group, the electric organ derives from striated muscle cells that suppress many muscle phenotypic properties (Bennett, 1971). Gymnotiforms have been used to study the formation of sensory and motor specializations (Fox and Richardson, 1978;Fox and Richardson, 1979;Kirschbaum and Schwassmann, 2008;Denizot et al, 1998;Denizot et al, 2007;Vischer, 1989a;Vischer, 1989b;Zakon, 1984;Lannoo et al, 1990), animal communication (Zakon et al, 2008;Carr and Friedman, 1999;Hopkins, 1988), speciation (Arnergard et al, 2010;Feulner et al, 2009;Lovejoy et al, 2010), evolution of neural networks (Alves-Gomes, 2001;Bass, 1986;Zakon et al, 2008;Kawasaki, 2009;Arnegard et al, 2010), physiology of membrane excitability and synaptic plasticity (Bell et al, 2005;Gómez et al, 2005;Lewis and Maler, 2004;Markham et al, 2009), and have been a source of material for the isolation of many molecules involved in these biological processes. Not as well known is the considerable regeneration capacity of South American gymnotiform electric fishes.…”

Section: Regeneration In Adult Gymnotiform Electric Fishmentioning

confidence: 99%

Electric fish: new insights into conserved processes of adult tissue regeneration

Unguez

2013

Journal of Experimental Biology

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SummaryBiology is replete with examples of regeneration, the process that allows animals to replace or repair cells, tissues and organs. As on land, vertebrates in aquatic environments experience the occurrence of injury with varying frequency and to different degrees. Studies demonstrate that ray-finned fishes possess a very high capacity to regenerate different tissues and organs when they are adults. Among fishes that exhibit robust regenerative capacities are the neotropical electric fishes of South America (Teleostei: Gymnotiformes). Specifically, adult gymnotiform electric fishes can regenerate injured brain and spinal cord tissues and restore amputated body parts repeatedly. We have begun to identify some aspects of the cellular and molecular mechanisms of tail regeneration in the weakly electric fish Sternopygus macrurus (long-tailed knifefish) with a focus on regeneration of skeletal muscle and the muscle-derived electric organ. Application of in vivo microinjection techniques and generation of myogenic stem cell markers are beginning to overcome some of the challenges owing to the limitations of working with non-genetic animal models with extensive regenerative capacity. This review highlights some aspects of tail regeneration in S. macrurus and discusses the advantages of using gymnotiform electric fishes to investigate the cellular and molecular mechanisms that produce new cells during regeneration in adult vertebrates.

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Ontogeny and evolution of electric organs in gymnotiform fish

Cited by 28 publications

References 11 publications

Electrocyte physiology: 50 years later

Electrocyte physiology: 50 years later

Old gene duplication facilitates origin and diversification of an innovative communication system—twice

Electric fish: new insights into conserved processes of adult tissue regeneration

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