Electrogenic fish – what’s in charge of the charge?

ResearchBlogging.org

Electric organs – organs that are capable of creating and discharging electricity – have evolved independently in at least six different lineages of fish (Torpediniformes, Rajiformes, Mormyroidea, Euteleostei, Siluriformes, Gymnotiformes) and play an important role in communication, navigation, defense and predation.

To investigate whether the convergent evolution of these organs has a common genetic basis, Jason Gallant and his coworkers studied the transcriptome of five species of electrogenic fish in three different lineages: Electrophorus electricus, Sternopygus macrurus, Eigenmannia virescens (Gymnotiforme), Malapterurus electricus (Siluriforme) and Brienomyrus brachyistius (Mormyroidea).

Electric organs are comprised of arrays of electrocytes – asymmetric cells that are enriched in cation-specific ion channels on one and sodium pumps on the opposing side. The resulting ion flux slowly charges the electrocyte membrane and upon activation by a neuronal stimulus, the voltage is discharged, generating an electrical pulse from the fish.

Although the morphology of electric organs and electrocytes varies substantially amongst these species, they are all muscle-derived tissue and originate developmentally from muscle progenitor cells.

Since this evolution of muscular to electrogenic tissue has occurred several times independently, the authors investigated, whether the underlying genetic mechanisms are shared.

To address this question, Gallant et al. first sequenced and assembled the genome of the electric eel, E. electricus. The authors further performed transcriptome analysis on multiple tissues of E. electricus as well as on pairs of skeletal muscle and electric organ tissue of two species within the same lineage (S. macrurus and E. virescens) and two species of distinct lineages (B. brachyistius, M. electricus).

Main findings

Across the species they observed common patterns of differential gene expression between electric organs versus skeletal muscles, which they attributed to the following five key mechanisms for the evolution of electrogenic tissue:

  • Alteration of the expression of myogenic transcription factors
  • Increased excitability by upregulation of transporters and ion channels
  • Enhanced isolation and direction of electrical currents by the upregulation of proteins in the connective tissue
  • Decrease in contractility by down-regulation of sarcomere associated genes
  • Increase of cell size by up-regulation of factors in the Insulin-like growth factor signaling pathway

Gallant et al. propose a convincing set of changes in gene expression to explain the functional differences between electric organ and muscle tissue. The fact that these mechanisms seem to be conserved in five species of electrogenic fish is an intriguing, yet not entirely surprising observation: presumably there are strong constraints on keeping muscle function intact while opening the potential for specialization to electric tissue – it would be interesting to inquire if – and to what extent – these shared expression differences are reflected on the genetic level.

Given the ambitious goal of uncovering the basis of electric organ evolution, I think the sampling of only one individual per species is problematic, despite the authors´ main interest in inter-species similarities. For an evolutionary approach the importance of intra-species variations should not be neglected and certainly requires a larger number of individuals. Including specimens from the other electrogenic lineages (e.g. Torpediniformes, Rajiformes) or (genetic) comparisons between electrogenic and non-electrogenic descendants within a lineage would have further strengthened the evolutionary aspect.

Lastly one could suspect that phylogenetically “older” electric organs have undergone a more advanced tissue specialization, resulting in a reduced “muscle profile” but the authors do neither raise this question, nor provide any information on this aspect.

Nevertheless I can highly recommend reading and discussing the paper – the ideas and methodology are presented in a clear language, the figures are appealing and – apart from the histological pictures – informative and well explained.

Although the results on what is in charge of the evolution of electric organs holds no shocking surprise yet, the research is still electrifying. 😉

Gallant, J., Traeger, L., Volkening, J., Moffett, H., Chen, P., Novina, C., Phillips, G., Anand, R., Wells, G., Pinch, M., Guth, R., Unguez, G., Albert, J., Zakon, H., Samanta, M., & Sussman, M. (2014). Genomic basis for the convergent evolution of electric organs Science, 344 (6191), 1522-1525 DOI: 10.1126/science.1254432

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