Signal variation and its morphological correlates in Paramormyrops kingsleyae provide insight into the evolution of electrogenic signal diversity in mormyrid electric fish

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 197, Issue 8, 2011, Pages 799-817

  Gallant, Jason R ^a   Arnegard, Matthew E ^b   Sullivan, John P ^a   Carlson, Bruce A ^c   Hopkins, Carl D ^a  

^a Cornell University ^*  (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

Biogeography; Electric organ; Electrocyte; Geographic variation; Signal evolution

Indexed keywords

EID: 85027919021     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-011-0643-8     Document Type: Article

References (57)

1. Alves-Gomes J, Hopkins CD (1997) Molecular insights into the phylogeny of mormyriform fishes and the evolution of their electric organs. Brain Behav Evol 49: 324-351.
2. Arnegard ME, Hopkins CD (2003) Electric signal variation among seven blunt-snouted Brienomyrus species (Teleostei: Mormyridae) from a riverine species flock in Gabon, Central Africa. Environ Biol Fishes 67: 321-339.
3. Arnegard ME, Jackson BS, Hopkins CD (2006) Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes. J Exp Biol 209: 2182-2198.
4. Arnegard ME, McIntyre PB, Harmon LJ, Zelditch ML, Crampton WGR, Davis JK, Sullivan JP, Lavoué S, Hopkins CD (2010) Sexual signal evolution outpaces ecological divergence during electric fish species radiation. Am Nat 176: 335-356.
5. Arnegard ME, Bogdanowicz SM, Hopkins CD (2005) Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry. Evolution 59: 324-343.
6. Baier B, Lamml M, Kramer B (2006) Ontogeny of the electric organ discharge in two parapatric species of the dwarf stonebasher, Pollimyrus castelnaui and P. marianne (Mormyridae, Teleostei). Acta Zool 87: 209-214.
7. Bass AH (1986a) A hormone-sensitive communication-system in an electric fish. J Neurobiol 17: 131-155.
8. Bass AH (1986b) Electric organs revisited: evolution of a vertebrate communication and orientation organ. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 13-70.
9. Bass AH (1986c) Species differences in electric organs of mormyrids: substrates for species-typical electric organ discharge waveforms. J Comp Neurol 244: 313-330.
10. Bass AH, Denizot JP, Marchaterre MA (1986) Ultrastructural features and hormone-dependent sex-differences of mormyrid electric organs. J Comp Neurol 254: 511-528.
11. Bass AH, Volman SF (1987) From behavior to membranes-testosterone-induced changes in action-potential duration in electric organs. Proc Natl Acad Sci USA 84: 9295-9298.
12. Bennett MV, Grundfest H (1961) Studies on morphology and electrophysiology of electric organs III. Electrophysiology of electric organs in mormyrids. In: Chagas C, Paes de Carvalho A (eds) Bioelectrogenesis pp 113-135.
13. Bennett MV (1971) Electric organs. In: Hoar W, Randall D (eds) Fish physiology, vol 5. Academic Press, New York, pp 347-491.
14. Bradbury JW, Verencamp SL (1998) Principles of animal communication, 1st edn. Sinauer Associates, New York.
15. Carlson BA (2009) Temporal-pattern recognition by single neurons in a sensory pathway devoted to social communication behavior. J Neurosci 29: 9417-9428.
16. Carlson BA (2002) Electric signaling behavior and the mechanisms of electric organ discharge production in mormyrid fish. J Physiol Paris 96: 405-419.
17. Caputi AA, Carlson BA, Macadar O (2005) Electric organs and their control. In: Bullock TH, Hopkins C, Popper A, Fay RR (eds) Electroreception. Springer, New York, pp 410-451.
18. Denizot JP, Kirschbaum F, Westby GWM, Tsuji S (1982) On the development of the adult electric organ in the mormyrid fish Pollimyrusisidori (with special focus on the innervation). J Neurocytol 11: 913-934.
19. Endler JA (1989) Conceptual and other problems in speciation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Associates, Sunderland, pp 625-648.
20. Feulner PG, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009) Electrifying love: electric fish use species-specific discharge for mate recognition. Biol Lett 23: 225-228.
21. Foster SA, Scott RJ, Cresko WA (1998) Nested biological variation and speciation. Philos Trans R Soc B 353: 207-218.
22. Xu-Friedman MA, Hopkins C (1999) Central mechanisms of temporal analysis in the knollenorgan pathway of mormyrid electric fish. J Exp Biol 202: 1311-1318.
23. Günther A (1896) Report on a collection of reptiles and fishes made by Miss M. H. Kingsley during her travels on the Ogowe river and in Old Calabar. Ann Mag Nat Hist 100: 261-285.
24. Hopkins CD (1980) Evolution of electric communication channels of mormyrids. Behav Ecol Sociobiol 7: 1-13.
25. Hopkins CD (1986) Behavior of mormyridae. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 527-576.
26. Hopkins CD (1999) Signal evolution in electric communication. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, pp 461-491.
27. Hopkins CD, Bass AH (1981) Temporal coding of species recognition signals in an electric fish. Science 212(4490): 85-87.
28. Hopkins CD, Lavoué S, Sullivan JP (2007) Mormyridae. In: Stiassny MLJ, Teugels GG, Hopkins CD (eds) Poissons D'eaux Douces Et Saumâtres De Basse Guinée: Ouest de l'Afrique Centrale vol 1. Faune Et Flore Tropicales. IRD Éditions, Paris, pp 220-334.
29. Iles RB (1960) External sexual differences, their significance in Mormyrus kannume (Forskal, 1775). Nature 188: 516.
30. Kirschbaum F (1995) Reproduction and development in mormyriform and gymnotiform fishes. In: Moller P (ed) Electric fishes: history and behavior. Chapman & Hall, London, pp 267-301.
31. Kramer B, Westby GWM (1985) No sex difference in the waveform of the pulse type electric fish, Gnathonemus petersii (Mormyridae). J Comp Physiol A 145: 399-403.
32. Kramer B, van der Bank H (2000) The southern churchill, Petrocephalus wesselsi, a new species of mormyrid from South Africa defined by electric organ discharges, genetics, and morphology. Environ Biol Fish 59: 393-413.
33. Kramer B, van der Bank H, Flint N, Sauer-Gürth H, Wink M (2003) Evidence for parapatric speciation in the mormyrid fish Pollimyrus castelnaui (Boulenger, 1911) from the Okavango-Upper Zambezi river systems: P. marianne sp. nov., defined by electric organ discharges, morphology and genetics. Environ Biol Fish 67: 47-70.
34. Kramer B, van der Bank H, Wink M (2004) Hippopotamyrus ansorgii species complex in the upper Zambezi River system with a description of a new species, H. szaboi (Mormyridae). Zool Scr 33: 1-18.
35. Kramer B, Skelton P, van der Bank H, Wink M (2007) Allopatric differentiation in the Marcusenius macrolepidotus species complex in Southern and Eastern Africa: the resurrection of M. pongolensis and M. angolensis, and the description of two new Species (Mormyridae, Teleostei). J Nat Hist 41: 647-708.
36. Kramer B, Swartz E (2010) Hippopotamyrus ansorgii complex from the Cunene river in southern Africa (Teleostei: Mormyriformes). J Nat Hist 44: 2213-2242.
37. Lamml M, Kramer B (2006) Differentiation of courtship songs in parapatric sibling species of dwarf stonebashers from southern Africa (Mormyridae, Teleostei). Behavior 143: 783-810.
38. Lamml M, Kramer B (2007) Allopatric differentiation in the acoustic communication of a weakly electric fish from southern Africa, Marcusenius macrolepidotus (Mormyridae, Teleostei) Behav Ecol Sociobiol 61: 385-399.
39. Lavoué S, Arnegard ME, Sullivan JP, Hopkins CD (2008) Petrocephalus of Odzala offer insights into evolutionary patterns of signal diversification in the Mormyridae, a family of weakly electrogenic fishes from Africa. J Physiol Paris 102: 322-339.
40. Lévêque D, Paugy D, Teugels GG (1990) The fresh and brackish water fishes of West Africa, vol 1. Musée Royal de l'Afrique Centrale, Tervuren.
41. Lewontin RC (1974) The genetic basis for evolutionary change. Columbia University Press, New York.
42. Machnik P, Kramer B (2008) Female choice by electric pulse duration: attractiveness of the males' communication signal assessed by female bulldog fish, Marcusenius pongolensis (Mormyridae, Teleostei). J Exp Biol 211: 1969-1977.
43. Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge.
44. McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of southwestern British Columbia. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford.
45. Meyer JH (1982) Behavioral responses of weakly electric fish to complex impedances. J Comp Physiol A 145: 459-470.
46. Pezzanite B, Moller P (1998) A sexually dimorphic basal anal-fin ray expansion in the weakly discharging electric fish Gnathonemus petersii. J Fish Biol 53: 638-644.
47. Pfenning KS, Pfenning DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Q Rev Biol 84: 253-276.
48. Protas M, Conrad M, Gross JB, Tabin C, Borowsky R (2007) Regressive evolution in the Mexican cave tetra, Astyanax mexicanus. Curr Biol 17: 452-454.
49. Scheffel A, Kramer B (1997) Electrocommunication and social behavior in Marcusenius senegalensis (Mormyridae, Teleostei). Ethology 103: 404-420.
50. Sullivan JP, Lavoué S, Arnegard ME, Hopkins CD (2004) AFLPs resolve phylogeny and reveal mitochondrial introgression within a species flock of African electric fish (Mormyroidea: Teleostei). Evolution 58: 825-841.
51. Sullivan JP, Lavoué S, Hopkins CD (2000) Molecular systematics of the African electric fishes (Mormyroidea: Teleostei) and a model for the evolution of their electric organs. J Exp Biol 203: 665-683.
52. Sullivan JP, Lavoué S, Hopkins CD (2002) Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 56: 597-616.
53. Szabo T (1960) Development of the electric organ of Mormyridae. Nature 188: 760-762.
54. Teugels G, Hopkins CD (1998) Morphological and osteological evidence for the generic position of Mormyrus kingsleyae in the genus Brienomyrus (Teleostei: Mormyridae). Copeia 1998: 199-204.
55. Verrell PA (1998) Geographic variation in sexual behavior: sex, signals and speciation. In: Foster SA, Endler JA (eds) The evolution of geographic variation in behavior. Oxford University Press, Oxford.
56. von der Emde G (1999) Active electrolocation of objects in weakly electric fish. J Exp Biol 202: 1205-1215.
57. Werneyer M, Kramer B (2006) Ontogenetic development of electric-organ discharges in a mormyrid fish, the bulldog Marcusenius macrolepidotus (South African Form). J Fish Biol 69: 1190-1201.