Environmental Biology of Fishes

, Volume 67, Issue 1, pp 47–70 | Cite as

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

  • Bernd Kramer
  • Herman van der Bank
  • Nicolette Flint
  • Hedi Sauer-Gürth
  • Michael Wink
Article

Abstract

We report on parapatric speciation in the mormyrid fish, Pollimyrus castelnaui (Boulenger, 1911), from the Okavango and the Upper Zambezi River systems. We recognise samples from the Zambezi River as a distinct species, P. marianne, displaying an eastern phenotype of electric organ discharge (EOD) waveform (Type 3) that is distinct from the western EOD phenotype (Type 1) observed in P. castelnaui samples from the neighbouring Okavango. Samples from the geographically intermediate Kwando/Linyanti River (a tributary of the Zambezi that is also intermittently connected to the Okavango) presented a more variable third EOD phenotype (Type 2). In 13 out of 14 morphological characters studied, the Zambezi River samples differed significantly from P. castelnaui. Morphologically and in EOD characters, the Kwando/Linyanti fish are distinct from both P. castelnaui and P. marianne. Sequence analysis of the mitochondrial cytochrome b gene unambiguously reveals that specimens from the Zambezi River System form a well supported taxon which clearly differs from P. castelnaui from the Okavango (1.5–2.5% sequence divergence). Within specimens from the Kwando–Zambezi System some geographic differentiation can be detected (nucleotide substitutions up to 0.6%); but groups cannot be resolved with certainty. Significant allozyme differences were found between the Okavango and all other EOD types from the Upper Zambezi System, and, within the Zambezi System, between the Kwando (Type 2) and Zambezi (Type 3) individuals. The low Wright's fixation index values, the lack of fixed allele differences, and small genetic distances provide little evidence for speciation between groups within the Zambezi System, but moderate to great fixation index values and significant allele frequency differences were observed between the Okavango and the other fishes. It is concluded that within the Zambezi System, differentiation between Kwando/Linyanti and Zambezi populations (as revealed by morphology and EOD waveform comparisons) is so recent that substantial genetic (allozyme and mitochondrial sequence) differences could not have evolved, or were not detected.

allozymes mitochondrial DNA behaviour cytochrome b sequence analysis clinal variation phylogeny phylogeography Caprivi Strip 

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References cited

  1. Alves-Gomes, J. & C.D. Hopkins. 1997. Molecular insights into the phylogeny of Mormyriform fishes and the evolution of their electric organs. Brain Behav. Evol. 49: 324-351.Google Scholar
  2. Bass, A.H. 1986. Electric organs revisited: evolution of a vertebrate communication and orientation organ. pp. 13-70. In: T.H. Bullock & W. Heiligenberg (ed.) Electroreception, John Wiley, New York.Google Scholar
  3. Bennett, M.V.L. 1971. Electric organs. pp. 347-491. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol 5, Academic Press, New York.Google Scholar
  4. Bell-Cross, G. & J.L. Minshull. 1988. The fishes of Zimbabwe. Harare: National Museums and Monuments of Zimbabwe. 294 pp.Google Scholar
  5. Boulenger, G.A. 1911. On a collection of fishes from the Lake Ngami basin. Trans. Zool. Soc. 18: 399-430.Google Scholar
  6. Bratton, B.O. & B. Kramer. 1988. Intraspecific variability of the pulse-type discharges of the African electric fishes, Pollimyrus isidori and Petrocephalus bovei (Mormyridae, Teleostei), and their dependence on water conductivity. Exp. Biol. 47: 227-238.Google Scholar
  7. Bratton, B.O. & B. Kramer. 1989. Patterns of the electric organ discharge during courtship and spawning in the mormyrid Pollimyrus isidori. Behav. Ecol. Sociobiol. 24: 349-368.Google Scholar
  8. Carvalho, G.R. & L. Hauser. 1999. Molecular markers and the species concept: New techniques to resolve old disputes? Rev. Fish Biol. Fish. 9: 379-382.Google Scholar
  9. Cockburn, A. 1991. An Introduction to Evolutionary Ecology. Blackwell Scientific Publications, London. 370 pp.Google Scholar
  10. Cook, L.M. 1991. Genetic and Ecological Diversity: The Sport of Nature. Chapman & Hall, London. 208 pp.Google Scholar
  11. Crawford, J.D. 1991. Sex recognition by electric cues in a sound-producing mormyrid fish, Pollimyrus isidori. Brain Behav. Evol. 38: 20-38.Google Scholar
  12. Desjardins, P. & R. Morais. 1990. Sequence and gene organisation of chicken mitochondrial genome. J. Mol. Biol. 212: 599-634.Google Scholar
  13. Futuyma, D.J. 1998. Evolutionary Biology 3rd edn. Sinauer, Sunderland. 763 pp.Google Scholar
  14. Gosse, J.-P. 1984. Mormyriformes. pp. 63-124. In: J. Daget, J.-P. Gosse, & D.F.E. Thys van den Audenaerde (ed.) Check-list of the Freshwater Fishes of Africa, Vol 1, ORSTOM/MRAC, Bondy (France)/Tervuren (Belgium).Google Scholar
  15. Graff, C. & B. Kramer. 1992. Trained weakly-electric fishes Pollimyrus isidori and Gnathonemus petersii (Mormyridae, Teleostei) discriminate between waveforms of electric pulse discharges. Ethology 90: 279-292.Google Scholar
  16. Grobler, H.J.W. 1987. 'n Visekologiese studie van die Liambezimeer in Caprivi, Suidwes-Afrika. (A Fish-ecological Study on Lake Liambezi in Caprivi, South-West Africa). M.Sc. dissertation, Rand Afrikaans University, Auckland Park (South Africa). 139 pp.Google Scholar
  17. Heidrich, P., C. König & M. Wink. (1995). Bioakustik, Taxonomie und molekulare Systematik amerikanischer Sperlingskäuze (Strigidae: Glaucidium spp.). Stuttgarter Beiträge zur Naturkunde A, 534: 1-47.Google Scholar
  18. Jubb, R.A. 1958. A preliminary report on the collections of freshwater fishes made by the Bernard Carp expeditions to the Caprivi Strip, 1949, the lower Sabi River, 1950, and to Barotseland, 1952. Occasional Papers of the National Museums of Southern Rhodesia 3(22b): 177-189.Google Scholar
  19. Kocher, T.D. & C.A. Stepien. 1997. Molecular Systematics of Fishes. Academic Press, San Diego. 520 pp.Google Scholar
  20. Kocher, T.D., W.K. Thomas, A. Meyer, S.V. Edwards, S. Pääbo, F.X. Villablanca & A.C. Wilson. 1989. Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86: 6196-6200.Google Scholar
  21. Kornfield, I. 1978. Evidence for rapid speciation in African cichlid fishes. Experientia 34: 335-336.Google Scholar
  22. Kramer, B. 1990. Electrocommunication in Teleost Fishes: Behavior and Experiments. Springer-Verlag, Berlin. 240 pp.Google Scholar
  23. Kramer, B. 1996. Electroreception and Communication in Fishes. Gustav Fischer Verlag, Stuttgart. 119 pp.Google Scholar
  24. Kramer, B. 1997a. Electric organ discharges and their relation to sex in mormyrid fishes. Naturwissenschaften 84: 119-121.Google Scholar
  25. Kramer, B. 1997b. A field study of African elephant-fish (Mormyridae, Teleostei): electric organ discharges in Marcusenius macrolepidotus (Peters, 1852) and Petrocephalus catostoma (Günther, 1866) as related to sex. J. Afr. Zool. 111: 313-341.Google Scholar
  26. Kramer, B. & B. Kuhn. 1993. Electric signalling and impedance matching in a variable environment: the electric organ of a mormyrid fish actively adapts to changes in water conductivity. Naturwissenschaften 80: 43-46.Google Scholar
  27. Kramer, B. & F.H. Van der Bank. 2000. The southern churchill (Petrocephalus wesselsi), a new species of mormyrid from South Africa defined by electric organ discharges, genetics, and morphology. Environ. Biol. Fishes 59: 393-413.Google Scholar
  28. Kramer, B., F.H. Van der Bank & M. Wink. 2003. Hippopotamyrus ansorgii species complex in the Upper Zambezi River System with a description of a new species, H. szaboi (Mormyridae). Zool. Scripta 32: in press.Google Scholar
  29. Kramer, B. & G.W.M. Westby. 1985. No sex difference in the waveform of the pulse type electric fish, Gnathonemus petersii (Mormyridae). Experientia 41: 1530-1531.Google Scholar
  30. Lavoué, S., R. Bigorne, G. Lecointre, & J.-F. Agnèse. 2000. Phylogenetic relationships of mormyrid electric fishes (Mormyridae; Teleostei) inferred from cytochrome b sequences. Mol. Phylogenet. Evol. 14: 1-10.Google Scholar
  31. Leviton, A.E., R.H. Gibbs, E. Heal, & C.E. Dawson 1985. Standards in herpetology and ichthyology: part I. Standard symbolic codes for institutional resource collections in herpetology and ichthyology. Copeia 1985: 802-832.Google Scholar
  32. Lissmann, H.W. 1958. On the function and evolution of electric organs in fish. J. Exp. Biol. 35: 156-191.Google Scholar
  33. Mayr, E. 1970. Populations, Species, and Evolution: An Abridgement of Animal Species and Evolution. Belknap Press, Boston. 453 pp.Google Scholar
  34. Meyer, A., D.T. Kocher, P. Basasibwaki & A.C. Wilson. 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347: 550-553.Google Scholar
  35. Moller, P. 1995. Electric Fishes: History and Behavior. Chapman & Hall, London. 584 pp.Google Scholar
  36. Nei, M. 1973. Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA. 70: 3321-3323.Google Scholar
  37. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.Google Scholar
  38. Pääbo, S. 1990. Amplifying ancient DNA. pp. 159-166. In: M.A. Innes, D.H. Gelfand, J.J. Sninsky & T.J. White (ed.). PCR Protocols: A Guide to Methods and Applications, Academic Press, San Diego.Google Scholar
  39. Paintner, S. (1998) Elektrosensorische Grundlagen der Impulskurvenformanalyse für die Individualerkennung bei Pollimyrus adspersus (Mormyridae, Teleostei). Ph.D. Dissertation, University of Regensburg.Google Scholar
  40. Paintner, S. & B. Kramer. In preparation. Electrosensory basis for individual recognition in a weakly electric, mormyrid fish, Pollimyrus adspersus (Günther, 1866).Google Scholar
  41. Schlettwein, C.H.G. 1985a. Third annual report on the hydrology of the Eastern Caprivi. Unpublished Report. Department of Water Affairs, South-West Africa. 27 pp.Google Scholar
  42. Schlettwein, C.H.G. 1985b. The biological control of Salvinia molesta. Unpublished Report. Department of Water Affairs, South-West Africa. 19 pp.Google Scholar
  43. Shaklee, J.B., C.S. Tamaru & R.S. Waples. 1982. Speciation and evolution of marine fishes studied by electrophoretic analysis of proteins. Pac. Sci. 36: 141-157.Google Scholar
  44. Skelton, P.H. 2001. A complete guide to the freshwater fishes of southern Africa. 2nd edn. Struik Publishers, Cape Town. 395 pp. (1st edn. 1993).Google Scholar
  45. Skelton, P.H., M.N. Bruton, G.S. Merron & B.C.W. van der Waal. 1985. The fishes of the Okavango drainage system in Angola, South West Africa and Botswana: taxonomy and distribution. Ichthyol. Bull. J.L.B. Smith Inst. Ichthyol. 50: 1-21.Google Scholar
  46. Stiassny, M.L.J. & A. Meyer. 1999. Cichlids of the Rift Lakes. Sci. Am. 280(2): 44-49.Google Scholar
  47. Sullivan, J.P., S. Lavoué & C.D. Hopkins. 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.Google Scholar
  48. Swofford, D.L. 2001. PAUP*. Phylogenetic analysis using parsimony (and other methods). Version 4.0b8. Sinauer Associates, Sunderland. (Software with user's manual, 257 pp).Google Scholar
  49. Swofford, D.L., R.B. Selander & W.C. Black. 1997. BIOSYS-2: A computer program for the analysis of allelic variation in genetics. Department of genetics and development. University of Illinois at Urbana-Champaign, Urbana, Illinois 60801, U.S.A. (Software with user's manual, 64 pp).Google Scholar
  50. Szabo, T. 1974. Anatomy of the specialized lateral line organs of electroreception. pp. 13-58. In: A. Fessard (ed.) Handbook of Sensory Physiology, Vol III/3, Springer-Verlag, Berlin.Google Scholar
  51. Szabo, T. & A. Fessard. 1974. Physiology of electroreceptors. pp. 59-124. In: A. Fessard (ed.) Handbook of Sensory Physiology, Vol III/3, Springer-Verlag, Berlin, Heidelberg, New York.Google Scholar
  52. Taverne, L. 1971. Ostéologie des genres Marcusenius Gill, Hippopotamyrus Pappenheim, Cyphomyrus Myers, Pollimyrus Taverne et Brienomyrus Taverne (Pisces Mormyriformes). Ann. Mus. R. Afr. Cent. Zool. 188: 1-144.Google Scholar
  53. Thorpe, J.P. 1982. The molecular clock hypothesis: Biochemical evolution, genetic differentiation and systematics. Ann. Rev. Ecol. Syst. 13: 139-168.Google Scholar
  54. Thorpe, J.P. & A.M. Solé-Cava. 1994. The use of allozyme electrophoresis in invertebrate systematics. Zool. Scripta 23: 3-18.Google Scholar
  55. Turner, G.F. 1999. What is a fish species? Rev. Fish Biol. Fish. 9: 281-297.Google Scholar
  56. Turner, R.W., L. Maler & M. Burrows (ed.). 1999. Electroreception and electrocommunication. J. Exp. Biol. 202: 1167-1458.Google Scholar
  57. Van der Bank, F.H. 1996. Inter-and intraspecific allozyme comparisons of mormyrids (Pisces, Mormyridae) from South Africa and Namibia, with reference to an undescribed species. Water SA 22(3): 285-290.Google Scholar
  58. Van der Bank, F.H. & B. Kramer. 1996. Phylogenetic relationships between eight African species of mormyriform fish (Teleostei, Osteichthyes): Resolution of a cryptic species, and reinstatement of Cyphomyrus Myers, 1960. Biochem. Syst. Ecol. 24: 275-291.Google Scholar
  59. Van der Bank, F.H. & M. van der Bank. 1995. An estimate of the amount of genetic variation in the snoutfish Marcusenius macrolepidotus (Peters, 1852). Water SA 21: 265-268.Google Scholar
  60. Van der Waal, B.C.W. 1978. 'n Visekologiese studie van die Liambezimeer in die Oos-Caprivi met verwysing na visontgunning deur die Bantoebevolking (A fish-ecological study of the Liambezi Lake in the Eastern Caprivi with reference to subsistance fishing by the native Bantu people). Ph.D. Dissertation, Rand Afrikaans University. 192 pp.Google Scholar
  61. Van der Waal, B.C.W. & P.H. Skelton. 1984. Check-list of fishes of Caprivi. Madoqua 13: 303-320.Google Scholar
  62. Verheyen, E. & J. van Rompaey. 1986. Genetics and speciation in African lacustrine cichlids. Ann. Mus. R. Afr. Centr. Zool. 251: 95-101.Google Scholar
  63. Wilson, A.C., H. Ochmann & E.M. Prager. 1987. Molecular time scale for evolution. Trends Genetics 3: 241-247.Google Scholar
  64. Wright, S. 1978. Evolution and the Genetics of Populations (Vol 4): Variability Within and Among Natural Populations. University of Chicago Press, Chicago. 590 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Bernd Kramer
    • 1
  • Herman van der Bank
    • 2
  • Nicolette Flint
    • 2
  • Hedi Sauer-Gürth
    • 3
  • Michael Wink
    • 3
  1. 1.Zoologisches InstitutUniversität RegensburgRegensburgGermany
  2. 2.Zoology DepartmentRand Afrikaans UniversityAuckland ParkSouth Africa
  3. 3.Universität HeidelbergHeidelbergGermany

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