Journal of Comparative Physiology A

, Volume 203, Issue 3, pp 183–195 | Cite as

Electric organ discharge diversification in mormyrid weakly electric fish is associated with differential expression of voltage-gated ion channel genes

  • Rebecca Nagel
  • Frank Kirschbaum
  • Ralph TiedemannEmail author
Original Paper


In mormyrid weakly electric fish, the electric organ discharge (EOD) is used for species recognition, orientation and prey localization. Produced in the muscle-derived adult electric organ, the EOD exhibits a wide diversity across species in both waveform and duration. While certain defining EOD characteristics can be linked to anatomical features of the electric organ, many factors underlying EOD differentiation are yet unknown. Here, we report the differential expression of 13 Kv1 voltage-gated potassium channel genes, two inwardly rectifying potassium channel genes, two previously studied sodium channel genes and an ATPase pump in two sympatric species of the genus Campylomormyrus in both the adult electric organ and skeletal muscle. Campylomormyrus compressirostris displays a basal EOD, largely unchanged during development, while C. tshokwe has an elongated, putatively derived discharge. We report an upregulation in all Kv1 genes in the electric organ of Campylomormyrus tshokwe when compared to both skeletal muscle and C. compressirostris electric organ. This pattern of upregulation in a species with a derived EOD form suggests that voltage-gated potassium channels are potentially involved in the diversification of the EOD signal among mormyrid weakly electric fish.


Weakly electric fish Ion channels Electric organ Gene expression Campylomormyrus 



Electric organ discharge


Genomic DNA


Quantitative reverse transcription PCR


RNA integrity number



We would like to thank Klaudia Manteuffel and Tonio Pieterek for care of the fish. We thank Linh Nguyen for providing juvenile EOD recordings. The work was supported by the University of Potsdam and GENART. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

359_2017_1151_MOESM1_ESM.pdf (11 kb)
Supplementary material 1 (PDF 10 KB)


  1. Abbas L, Hajihashemi S, Stead LF, Cooper GJ, Ware TL, Munsey TS, Whitfield TT, White SJ (2011) Functional and developmental expression of a zebrafish Kir1.1 (ROMK) potassium channel homologue Kcnj1. J Physiol 589:1489–1503. doi: 10.1113/jphysiol.2010.200295 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alves-Gomes JA (2001) The evolution of electroreception and bioelectrogenesis in teleost fish: a phylogenetic perspective. J Fish Biol 58:1489–1511. doi: 10.1006/jfbi.2001.1625 CrossRefGoogle Scholar
  3. Alves-Gomes JA, Hopkins CD (1997) Molecular insights into the phylogeny of mormyriform fishes and the evolution of their electric organs. Brain Behav Evol 49:324–350. doi: 10.1159/000316291 CrossRefPubMedGoogle Scholar
  4. Arnegard ME, Zwickl DJ, Lu Y, Zakon HH (2010) Old gene duplication facilitates origin and diversification of an innovative communication system–twice. Proc Natl Acad Sci USA 107:22172–22177. doi: 10.1073/pnas.1011803107 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bass AH (1986a) Electric organs revisited: evolution of a vertebrate communication and orientation organ. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13–70Google Scholar
  6. Bass AH (1986b) Species differences in electric organs of mormyrids: substrates for species-typical electric organ discharge waveforms. J Comp Neurol 244:313–330. doi: 10.1002/cne.902440305 CrossRefPubMedGoogle Scholar
  7. Bennett MVL (1971) Electric organs. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 5. Academic Press, New York, pp 347–491Google Scholar
  8. Brawand D, Soumillon M, Necsulea A, Julien P, Csárdi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, Albert FW, Zeller U, Khaitovich P, Grützner F, Bergmann S, Nielsen R, Pääbo S, Kaessmann H (2011) The evolution of gene expression levels in mammalian organs. Nature 478:343–348. doi: 10.1038/nature10532 CrossRefPubMedGoogle Scholar
  9. Budhia S, Haring LF, McConnell I, Blacklaws BA (2006) Quantitation of ovine cytokine mRNA by real-time RT-PCR. J Immunol Methods 309:160–172. doi: 10.1016/j.jim.2005.12.006 CrossRefPubMedGoogle Scholar
  10. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett JF, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. doi: 10.1373/clinchem.2008.112797 CrossRefPubMedGoogle Scholar
  11. Carroll SB (2008) Evo-Devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36. doi: 10.1016/j.cell.2008.06.030 CrossRefPubMedGoogle Scholar
  12. Denizot JP, Kirschbaum F, Westby GWM, Tsuji S (1982) On the development of the adult electric organ in the mormyrid fish Pollimyrus isidori (with special focus on the innervation). J Neurocytol 11:913–934. doi: 10.1007/BF01148308 CrossRefPubMedGoogle Scholar
  13. Denizot JP, Kirschbaum F, Schugardt C, Bensouilah M (1998) Larval electroreceptors indicate a larval electric system in mormyrids. Neurosci Lett 241:103–106. doi: 10.1016/S0304-3940(98)00030-5 CrossRefPubMedGoogle Scholar
  14. Ferrari MB, Zakon HH (1993) Conductances contributing to the action potential of Sternopygus electrocytes. J Comp Physiol A 173:281–292. doi: 10.1007/BF00212692 CrossRefPubMedGoogle Scholar
  15. Ferrari MB, McAnelly ML, Zakon HH (1995) Individual variation in and androgen-modulation of the sodium current in electric organ. J Neurosci 15:4023–4032PubMedGoogle Scholar
  16. Feulner PGD, Kirschbaum F, Schugardt C, Ketmaier V, Tiedemann R (2006) Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus). Mol Phylogenet Evol 39:198–208. doi: 10.1016/j.ympev.2005.09.008 CrossRefPubMedGoogle Scholar
  17. Feulner PGD, Kirschbaum F, Mamonekene V, Ketmaier V, Tiedemann R (2007) Adaptive radiation in African weakly electric fish (Teleostei: Mormyridae: Campylomormyrus): a combined molecular and morphological approach. J Evol Biol 20:403–414. doi: 10.1111/j.1420-9101.2006.01181.x CrossRefPubMedGoogle Scholar
  18. Feulner PGD, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009a) Electrifying love: electric fish use species-specific discharge for mate recognition. Biol Lett 5:225–228. doi: 10.1098/rsbl.2008.0566 CrossRefPubMedGoogle Scholar
  19. Feulner PGD, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009b) Magic trait electric organ discharge (EOD): dual function of electric signals promotes speciation in African weakly electric fish. Commun Integr Biol 2:329–331. doi: 10.1098/rsbl.2008.0566.for CrossRefPubMedPubMedCentralGoogle Scholar
  20. Few WP, Zakon HH (2007) Sex differences in and hormonal regulation of Kv1 potassium channel gene expression in the electric organ: molecular control of a social signal. Dev Neurobiol 67:535–549. doi: 10.1002/dneu.20305 CrossRefPubMedGoogle Scholar
  21. Fountain SJ, Cheong A, Flemming R, Mair L, Sivaprasadarao A, Beech DJ (2004) Functional up-regulation of KCNA gene family expression in murine mesenteric resistance artery smooth muscle. J Physiol 556:29–42. doi: 10.1113/jphysiol.2003.058594 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gallant JR, Hopkins CD, Deitcher DL (2012) Differential expression of genes and proteins between electric organ and skeletal muscle in the mormyrid electric fish Brienomyrus brachyistius. J Exp Biol 215:2479–2494. doi: 10.1242/jeb.063222 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gallant JR, Traeger LL, Volkening JD, Moffett H, Chen P-H, Novina CD, Phillips GN, Anand R, Wells GB, Pinch M, Güth R, Unguez GA, Albert JS, Zakon HH, Samanta MP, Sussman MR (2014) Genomic basis for the convergent evolution of electric organs. Science 644:1522–1525. doi: 10.1126/science.1254432 CrossRefGoogle Scholar
  24. Hibbeler S, Scharsack JP, Becker S (2008) Housekeeping genes for quantitative expression studies in the three-spined stickleback Gasterosteus aculeatus. BMC Mol Biol 9:18. doi: 10.1186/1471-2199-9-18 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hoegg S, Brinkmann H, Taylor JS, Meyer A (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203. doi: 10.1007/s00239-004-2613-z CrossRefPubMedGoogle Scholar
  26. Jan LY, Jan YN (1997) Voltage-gated and inwardly rectifying potassium channels. J Physiol 505:267–282. doi: 10.1111/j.1469-7793.1997.267bb.x CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kaiser P, Rothwell L, Galyov EE, Barrow PA, Burnside J, Wigley P (2000) Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. Microbiol 146:3217–3226. doi: 10.1099/00221287-146-12-3217 CrossRefGoogle Scholar
  28. Kirschbaum F (1977) Electric-organ ontogeny: distinct larval organ precedes the adult organ in weakly electric fish. Naturwissenschaften 64:387–388. doi: 10.1007/BF00368748 CrossRefGoogle Scholar
  29. Kirschbaum F (1983) Myogenic electric organ precedes the neurogenic organ in apteronotid fish. Naturwissenschaften 70:205–207. doi: 10.1007/BF01047569 CrossRefPubMedGoogle Scholar
  30. Kirschbaum F, Schugardt C (1995) Vergleichende Daten zur Forpflanzungsbiologie von zwei Nilhechte-Arten (Mormyridae). In: Greven H, Riehl R (eds) Fortpflanzungsbiologie der Aquarienfische. Birgit Schmettkamp Verlag, Bornheim, pp 81–90Google Scholar
  31. Kirschbaum F, Schugardt C (2002) Reproductive strategies and developmental aspects in mormyrid and gymnotiform fishes. J Physiol Paris 96:557–566. doi: 10.1016/S0928-4257(03)00011-1 CrossRefPubMedGoogle Scholar
  32. Lamanna F, Kirschbaum F, Tiedemann R (2014) De novo assembly and characterization of the skeletal muscle and electric organ transcriptomes of the African weakly electric fish Campylomormyrus compressirostris (Mormyridae, Teleostei). Mol Ecol Resour 14:1222–1230. doi: 10.1111/1755-0998.12260 CrossRefPubMedGoogle Scholar
  33. Lamanna F, Kirschbaum F, Waurick I, Dieterich C, Tiedemann R (2015) Cross-tissue and cross-species analysis of gene expression in skeletal muscle and electric organ of African weakly-electric fish (Teleostei; Mormyridae). BMC Genomics 16:668. doi: 10.1186/s12864-015-1858-9 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lamanna F, Kirschbaum F, Ernst ARR, Feulner PGD, Momonekene V, Paul C, Tiedemann R (2016) Species delimination and phylogenetic relationships in a genus of African weakly-electric fishes (Osteoglossiformes, Mormyridae, Campylomormyrus). Mol Phyl Evol 101:8–18. doi: 10.1016/j.ympev.2016.04.035 CrossRefGoogle Scholar
  35. Lissmann HW (1958) On the function and evolution of electric organs in fish. J Exp Biol 35:156–191Google Scholar
  36. Markham MR, Kaczmarek LK, Zakon HH (2013) A sodium-activated potassium channel supports high-frequency firing and reduces energetic costs during rapid modulations of action potential amplitude. J Neurophysiol 109:1713–1723. doi: 10.1152/jn.00875.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  37. McAnelly ML, Zakon HH (2000) Coregulation of voltage-dependent kinetics of Na(+) and K(+) currents in electric organ. J Neurosci 20:3408–3414PubMedGoogle Scholar
  38. McCurley AT, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol 9:102. doi: 10.1186/1471-2199-9-102 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27:937–945. doi: 10.1002/bies.20293 CrossRefPubMedGoogle Scholar
  40. Moller P (1995) Electric fishes: history and behavior. 1st ed. Springer NetherlandsGoogle Scholar
  41. Nguyen L, Paul C, Mamonekene V, Bartsch P, Tiedemann R, Kirschbaum F (2017) Reproduction and development in some species of the weakly electric genus Campylomormyrus (Mormyridae, Teleostei). Env Biol Fish 100:49–68. doi: 10.1007/s10641-016-0554-1 CrossRefGoogle Scholar
  42. Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New YorkCrossRefGoogle Scholar
  43. Pattnaik BR, Asuma MP, Spott R, Pillers DAM (2012) Genetic defects in the hotspot of inwardly rectifying K+ (Kir) channels and their metabolic consequences: a review. Mol Genet Metab 105:64–72. doi: 10.1016/j.ymgme.2011.10.004 CrossRefPubMedGoogle Scholar
  44. Paul C, Mamonekene V, Vater M, Feulner PGD, Engelmann J, Tiedemann R, Kirschbaum F (2015) Comparative histology of the adult electric organ among four species of the genus Campylomormyrus (Teleostei: Mormyridae). J Comp Physiol A 201:357–374. doi: 10.1007/s00359-015-0995-6 CrossRefGoogle Scholar
  45. Paul C, Kirschbaum F, Mamonekene V, Tiedemann R (2016) Evidence for non-neutral evolution in a sodium channel gene in African weakly electric fish (Campylomormyrus, Mormyridae). J Mol Evol 83:61–77. doi: 10.1007/s00239-016-9754-8 CrossRefPubMedGoogle Scholar
  46. Pfaffl MW, Georgieva TM, Georgiev IP, Ontsouka E, Hageleit M, Blum JW (2002) Real-time RT-PCR quantification of insulin-like growth factor (IGF)-1, IGF-1 receptor, IGF-2, IGF-2 receptor, insulin receptor, growth hormone receptor, IGF-binding proteins 1, 2 and 3 in the bovine species. Domest Anim Endocrinol 22:91–102. doi: 10.1016/S0739-7240(01)00128-X CrossRefPubMedGoogle Scholar
  47. R Development Core Team (2008) R: a language and environment for statistical computingGoogle Scholar
  48. Rosati B, McKinnon D (2004) Regulation of ion channel expression. Circ Res 94:874–883. doi: 10.1161/01.RES.0000124921.81025.1F CrossRefPubMedGoogle Scholar
  49. RStudio Team (2015) RStudio: Integrated Development for RGoogle Scholar
  50. Salkoff L, Baker K, Butler A, Covarrubias M, Pak M, Wei A (1992) An essential “set” of K+ channels conserved in flies, mice and humans. Trends Neurosci 15:161–166. doi: 10.1016/0166-2236(92)90165-5 CrossRefPubMedGoogle Scholar
  51. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3. doi: 10.1186/1471-2199-7-3 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Schugardt C, Kirschbaum F (1998) Sozial- und Fortpflanzungsverhalten von Mormyriden (Nilhechten). In: Greven H, Riehl R (ed) Verhalten der Aquarienfische1. pp 87–98Google Scholar
  53. Schugardt C, Kirschbaum F (2004) Control of gonadal maturation and regression by experimental variation of environmental factors in the mormyrid fish, Mormyrus rume proboscirostris. Environ Biol Fishes 70:227–233. doi: 10.1023/B:EBFI.0000033340.49266.f3 CrossRefGoogle Scholar
  54. Smith GT, Zakon HH (2000) Pharmacological characterization of ionic currents that regulate the pacemaker rhythm in a weakly electric fish. J Neurobiol 42:270–286. doi: 10.1002/neu.20202 CrossRefPubMedGoogle Scholar
  55. Steinke D, Salzburger W, Braasch I, Meyer A (2006) Many genes in fish have species-specific asymmetric rates of molecular evolution. BMC Genomics 7. doi: 10.1186/1471-2164-7-20 PubMedPubMedCentralGoogle Scholar
  56. Sullivan J, Lavoue S, Hopkins CD (2016) Cryptomyrus: a new genus of Mormyridae (Teleostei, Osteoglossomorpha) with two new species from Gabon, West-Central Africa. Zookeys 561:117–150. doi: 10.3897/zookeys.561.7137 CrossRefGoogle Scholar
  57. Szabo T (1960) Development of the electric organ of Mormyridae. Nature 188:760–762. doi: 10.1038/188760b0 CrossRefPubMedGoogle Scholar
  58. Thompson A, Vo D, Comfort C, Zakon HH (2014) Expression evolution facilitated the convergent neofunctionalization of a sodium channel gene. Mol Biol Evol 31:1941–1955. doi: 10.1093/molbev/msu145 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tiedemann R, Feulner PGD, Kirschbaum F (2010) Electric organ discharge divergence promotes ecological speciation in sympatrically occurring African weakly electric fish (Campylomormyrus). In: Glaubrecht M (ed) Evolution in Action. Springer-Verlag, Berlin, pp 307–321CrossRefGoogle Scholar
  60. Udvardi MK, Czechowski T, Scheible W-R (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20:1736–1737. doi: 10.1105/tpc.108.061143 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Westby GWM, Kirschbaum F (1977) Emergence and development of the electric organ discharge in the mormyrid fish, Pollimyrus isidori. J Comp Physiol A 122:251–271. doi: 10.1007/BF00611894 CrossRefGoogle Scholar
  62. Zakon HH, Mcanelly L, Smith GT, Dunlap K, Lopreato G, Oestreich J, Few WP (1999) Plasticity of the electric organ discharge: implications for the regulation of ionic currents. J Exp Biol 202:1409–1416PubMedGoogle Scholar
  63. Zakon HH, Lu Y, Zwickl DJ, Hillis DM (2006) Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc Natl Acad Sci USA 103:3675–3680. doi: 10.1073/pnas.0600160103 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zakon HH, Zwickl DJ, Lu Y, Hillis DM (2008) Molecular evolution of communication signals in electric fish. J Exp Biol 211:1814–1818. doi: 10.1242/jeb.015982 CrossRefPubMedGoogle Scholar
  65. Zakon HH, Jost MC, Zwickl DJ, Lu Y, Hillis DM (2009) Molecular evolution of Na+ channels in teleost fishes. Integr Zool 4:64–74. doi: 10.1111/j.1749-4877.2008.00136.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Rebecca Nagel
    • 1
  • Frank Kirschbaum
    • 2
  • Ralph Tiedemann
    • 1
    Email author
  1. 1.Institute of Biochemistry and Biology, Unit of Evolutionary Biology/Systematic ZoologyUniversity of PotsdamPotsdamGermany
  2. 2.Faculty of Life Sciences, Albrecht Daniel Thaer-Institute of Agricultural and Horticultural Sciences, Unit of Biology and Ecology of FishesHumboldt University of BerlinBerlinGermany

Personalised recommendations