Electrophysiological and molecular genetic evidence for sympatrically occuring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus)

Molecular Phylogenetics and Evolution

Volumn 39, Issue 1, 2006, Pages 198-208

  Feulner, P G D ^a   Kirschbaum, F ^b,c   Schugardt, C ^c   Ketmaier, V ^a   Tiedemann, R ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Campylomormyrus; Cryptic species; Electric fish; EOD polymorphism; Microsatellite; Mormyridae; Ontogeny; Phylogeny

Indexed keywords

MICROSATELLITE DNA;

AFRICA; ANIMAL; ARTICLE; CLASSIFICATION; ELECTRIC FISH; ELECTRIC ORGAN; ELECTROPHYSIOLOGY; FEMALE; GENETICS; MALE; PHYLOGENY; PHYSIOLOGY;

AFRICA; ANIMALS; ELECTRIC FISH; ELECTRIC ORGAN; ELECTROPHYSIOLOGY; FEMALE; MALE; MICROSATELLITE REPEATS; PHYLOGENY;

CAMPYLOMORMYRUS; CAMPYLOMORMYRUS NUMENIUS; CAMPYLOMORMYRUS TAMANDUA; MORMYRIDAE; PISCES; TAMANDUA; TELEOSTEI;

EID: 33644997110     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2005.09.008     Document Type: Article

References (78)

1. J. Alves-Gomes, and C.D. Hopkins Molecular insights into the phylogeny of Mormyriform fishes and the evolution of their electric organs Brain Behav. Evol. 49 1997 324 350
2. M.E. Arnegard, S.M. Bogdanowicz, and C.D. Hopkins Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatry Evolution 59 2005 324 343
3. M. Barluenga, and A. Meyer The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Mol. Ecol. 13 2004 2061 2076
4. A.H. Bass Species differences in electric organs of mormyrids: substrates for species-typical electric organ discharge waveforms J. Comp. Neurobiol. 244 1986 313 330
5. J. Bastian Electrosensory organisms Phys. Today 47 1994 30 37
6. L. Baudouin, and P. Lebrun An operational Bayesian approach for the identification of sexually reproduced cross-fertilized populations using molecular markers Acta Horticultura 546 2001 81 94
7. B.O. Bratton, and B. Kramer Patterns of the electric organ discharge during courtship and spawning in the mormyrid fish, Pollimyrus isidori Behav. Ecol. Sociobiol. 24 1989 349 368
8. S. Chow, and K. Hazama Universal PCR primers for S7 ribosomal protein gene introns in fish Mol. Ecol. 7 1998 1255 1256
9. M. Clement, D. Posada, and K.A. Crandall TCS: a computer program to estimate gene genealogies Mol. Ecol. 9 2000 1657 1659
10. J.D. Crawford Sex recognition by electric cues in a sound-producing mormyrid fish, Pollimyrus isidori Brain Behav. Evol. 38 1991 20 38
11. J.D. Crawford Individual and sex specificity in the electric organ discharges of breeding mormyrid fish (Pollimyrus isidori) J. Exp. Biol. 164 1992 79 102
12. J.D. Crawford, and X.F. Huang Communication signals and sound production mechanisms of mormyrid electric fish J. Exp. Biol. 202 1999 1417 1426
13. J.P. Denizot, F. Kirschbaum, G.W.M. Westby, and S. Tsuji On the development of the adult electric organ in the Mormyrid fish Pollimyrus isidori (with special focus on the innervation) J. Neurocytol. 11 1982 913 934
14. M. Doebeli, and U. Dieckmann Evolutionary branching and sympatric speciation caused by different types of ecological interactions Am. Nat. 156 2000 S77 S101
15. L. Excoffier, P.E. Smouse, and J.M. Quattro Analysis of molecular variance inferred from metric distances among DNA haplotypes-application to human mitochondrial-DNA restriction data Genetics 131 1992 479 491
16. J.S. Farris, A.G. Kluge, and M.J. Eckardt A numerical approach to phylogenetic systematics Syst. Zool. 19 1970 172
17. P.G.D. Feulner, F. Kirschbaum, and R. Tiedemann Eighteen microsatellite loci for endemic African weakly electric fish (Campylomormyrus, Mormyridae) and their cross species applicability among related taxa Mol. Ecol. Notes. 5 2005 446 448
18. M.A. Friedman, and C.D. Hopkins Tracking individual mormyrid electric fish in the field using electric organ discharge waveforms Anim. Behav. 51 1996 391 407
19. J.-P. Gosse Mormyriformes J. Daget J.-P. Gosse D.F.E. Thys van den Audenaerde Check-List of The Freshwater Fishes of Africa vol. 1 1984 ORSTOM MRAC Tervuren Paris 63 124
20. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic acids symp. ser. 41, 95-98.
21. M. Hasegawa, H. Kishino, and T.A. Yano Dating of the human ape splitting by a molecular clock of mitochondrial-DNA J. Mol. Evol. 22 1985 160 174
22. C.D. Hopkins, and A.H. Bass Temporal coding of species recognition signals in an electric fish Science 212 1981 85 87
23. C.D. Hopkins Design features for electric communication J. Exp. Biol. 202 1999 1217 1228
24. J.P. Huelsenbeck, B. Rannala, and J.P. Masly Accommodating phylogenetic uncertainty in evolutionary studies Science 288 2000 2349 2350
25. M. Kirkpatrick, and V. Ravigne Speciation by natural and sexual selection: models and experiments Am. Nat. 159 2002 S22 S35
26. F. Kirschbaum Electric-organ ontogeny-distinct larval organ precedes adult organ in weakly electric fish Naturwissenschaften 64 1977 387 388
27. F. Kirschbaum Ontogeny of both larval electric organ and electromotoneurones in Pollimyrus isidori (Mormyridae, Teleostei) T. Szabo G. Czeh Advances in Physiological Sciences. Sensory Physiology of Aquatic Lower Vertebrates vol. 31 1981 Pergamon Press Oxford and New York 129 157
28. F. Kirschbaum, and C. Schugardt Reproductive strategies and developmental aspects in mormyrid and gymnotiform fishes J. Physiol.-Paris 96 2002 557 566
29. B. Kramer, and B. Kuhn Species recognition by the sequence of discharge intervals in weakly electric fishes of the genus Campylomormyrus (Mormyridae, Teleostei) Anim. Behav. 48 1994 435 445
30. R. Lande, O. Seehausen, and J.J.M. van Alphen Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish Genetica 112 2001 435 443
31. R.E. Landsman Sex-differences in external morphology and electric organ discharges in imported Gnathonemus petersii (Mormyriformes) Anim. Behav. 46 1993 417 429
32. B. Larget, and D.L. Simon Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees Mol. Biol. Evol. 16 1999 750 759
33. G.V. Lauder, and K.F. Liem The evolution and interrelationship of the actinopterygian fishes Bull. Mus. Comp. Zool. 150 1983 95 197
34. S. Lavoué, R. Bigorne, G. Lecointre, and J.F. Agnese Phylogenetic relationships of mormyrid electric fishes (Mormyridae; Teleostei) inferred from cytochrome b sequences Mol. Phylogenet. Evol. 14 2000 1 10
35. S. Lavoué, J.P. Sullivan, and C.D. Hopkins Phylogenetic utility of the first two introns of the S7 ribosomal protein gene in African electric fishes (Mormyroidea: Teleostei) and congruence with other molecular markers Biol. J. Linn. Soc. 78 2003 273 292
36. H.W. Lissman, and K.E. Machin The mechanism of object location in Gymnarchus niloticus and similar fish J. Exp. Biol. 35 1958 451 486
37. Lovell, P.V., Hopkins, C.D., Harned, G.D., 1997. The diversity of electric organ discharges found in eight species of Campylomormyrus electric fish (Mormyridae). In: Abstracts of the Annual Meeting of the Society of Neurosciences vol. 23, p.2.
38. B. Mau, and M.A. Newton Phylogenetic inference for binary data on dendograms using Markov chain Monte Carlo J. Comput. Graph. Stat. 6 1997 122 131
39. B. Mau, M.A. Newton, and B. Larget Bayesian phylogenetic inference via Markov chain Monte Carlo methods Biometrics 55 1999 1 12
40. T.C. Mendelson Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma) Evolution 57 2003 317 327
41. J.S. Nelson Fishes of The World 1994 John wiley New York
42. D. Paetkau, W. Calvert, I. Stirling, and C. Strobeck Microsatellite analysis of population-structure in Canadian polar bears Mol. Ecol. 4 1995 347 354
43. S.R. Palumbi Nucleic acids. II. The polymerase chain reaction D.M. Hillis C. Moritz B.K. Mable Molecular Systematics 1996 Sinauer Associates Sunderland, MA 205 248
44. S. Piry, A. Alapetite, J.M. Cornuet, D. Paetkau, L. Baudouin, and A. Estoup GENECLASS2: a software for genetic assignment and first-generation migrant detection J. Hered. 95 2004 536 539
45. M. Poll, J.-P. Gosse, and S. Orts Le genre Campylomormyrus Bleeker, 1874, étude systématique et description d'une espéce nouvelle (Pisces Mormyridae) Bulletin Institut Royal des Sciences Naturelles de Belgique Biologie 54 1982 1 44
46. D. Posada, and K.A. Crandall MODELTEST: testing the model of DNA substitution Bioinformatics 14 1998 817 818
47. J.K. Pritchard, M. Stephens, and P. Donnelly Inference of population structure using multilocus genotype data Genetics 155 2000 945 959
48. B. Rannala, and Z.H. Yang Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference J. Mol. Evol. 43 1996 304 311
49. B. Rannala, and J.L. Mountain Detecting immigration by using multilocus genotypes Proc. Natl. Acad. Sci. USA 94 1997 9197 9201
50. T.R. Roberts, and D.J. Stewart An ecological and systematic survey of fishes in the rapids of the lower Zaire or Congo river Bull. Mus. Comp. Zool. 147 1976 239 317
51. F. Ronquist, and J.P. Huelsenbeck MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 2003 1572 1574
52. N. Saitou, and M. Nei The neighbor-joining method-a new method for reconstructing phylogenetic trees Mol. Biol. Evol. 4 1987 406 425
53. U. Schliewen, K. Rassmann, M. Markmann, J. Markert, T. Kocher, and D. Tautz Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon Mol. Ecol. 10 2001 1471 1488
54. Schneider, S., Roessli, D., Excoffier, L., 2000. ARLEQUIN: a software for population genetics data version 2.000. Department of Anthropology, University of Geneva, Switzerland.
55. Schugardt, C., Kirschbaum, F., 1998. Sozial- und Fortpflanzungsverhalten von Mormyriden (Nilhechten). In: Greven, H., Riehl, R. (Eds.) Verhalten der Aquarienfische. Birgit Schmettkamp Verlag, Bornheim, vol Symposiumband, pp. 87-98.
56. C. Schugardt, and F. Kirschbaum Nilhechte des Campylomormyrus numenius-Formenkreises: Bemerkungen zur Ontogenese des Habitus, der elektrischen Entladung sowie zum Fortpflanzungsverhalten H. Greven R. Riehl Verhalten der Aquarienfische Vol. 2 2002 Birgit Schmettkamp Verlag Bornheim 137 146
57. O. Seehausen, J.J.M. van Alphen, and F. Witte Cichlid fish diversity threatened by eutrophication that curbs sexual selection Science 277 1997 1808 1811
58. O. Seehausen, and J.M. van Alphen Can sympatric speciation by disruptive sexual selection explain rapid evolution of cichlid diversity in Lake Victoria? Ecol. Lett. 2 1999 262 271
59. G. Seutin, B.N. White, and P.T. Boag Preservation of avian blood and tissue samples for DNA analyses Can. J. Zool. 69 1991 82 90
60. H. Shimodaira An approximately unbiased test of phylogenetic tree selection Syst. Biol. 51 2002 492 508
61. H. Shimodaira, and M. Hasegawa Multiple comparisons of log-likelihoods with applications to phylogenetic inference Mol. Biol. Evol. 16 1999 1114 1116
62. H. Shimodaira, and M. Hasegawa CONSEL: for assessing the confidence of phylogenetic tree selection Bioinformatics Application Notes 17 2001 1246 1247
63. J.P. Sullivan, S. Lavoué, and C.D. Hopkins Molecular systematics of the African electric fishes (Mormyroidea: Teleostei) and a model for the evolution of their electric organs J. Exp. Biol. 203 2000 665 683
64. J.P. Sullivan, S. Lavoué, and C.D. Hopkins Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei) Evolution 56 2002 597 616
65. K. Tamura, M. Nei, and S. Kumar Prospects for inferring very large phylogenies by using the neighbor-joining method Proc. Natl. Acad. Sci. USA 101 2004 11030 11035
66. Taverne, L., 1972. Ostéologie des genres Mormyrus Linné, Mormyrops Müller, Hyperopisus Gill, Isichthys Gill, Myomyrus Boulenger, Stomatorhinus Boulenger et Gymnarchus Cuvier considérations générales sur la systématique des poissons de l'ordre des Mormyriformes. MRAC, Tervuren.
67. E.B. Taylor, and J.D. McPhail Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus Proc. R. Soc. Lond. B 267 2000 2375 2384
68. A.R. Templeton, K.A. Crandall, and C.F. Sing A cladistic inference of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation Genetics 132 1992 619 633
69. G.S. van Doorn, A.J. Noest, and P. Hogeweg Sympatric speciation and extinction driven by environment dependent sexual selection Proc. R. Soc. Lond. B 265 1998 1915 1919
70. G.S. van Doorn, U. Dieckmann, and F.J. Weissing Sympatric speciation by sexual selection: A critical reevaluation Am. Nat. 163 2004 709 725
71. M.J.H. van Oppen, G.F. Turner, C. Rico, R.L. Robinson, J.C. Deutsch, M.J. Genner, and G.M. Hewitt Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi Mol. Ecol. 7 1998 991 1001
72. G. von der Emde Active electrolocation of objects in weakly electric fish J. Exp. Biol. 202 1999 1205 1215
73. B.S. Weir, and C.C. Cockerham Estimating F-statistics for the analysis of population structure Evolution 38 1984 1358 1370
74. M. Werneyer, and B. Kramer Intraspecific agonistic interactions in freely swimming mormyrid fish, Marcusenius macrolepidotus (South African form) J. Ethol. 20 2002 107 121
75. G.W.M. Westby, and F. Kirschbaum Emergence and development of electric organ discharge in Mormyrid fish, Pollimyrus isidori 1. Larval discharge J. Comp. Physiol. 122 1977 251 271
76. G.W.M. Westby, and F. Kirschbaum Emergence and development of electric organ discharge in Mormyrid fish, Pollimyrus isidori 2. Replacement of larval by adult discharge J. Comp. Physiol. 127 1978 45 59
77. G.W.M. Westby, and F. Kirschbaum Sex-differences in the waveform of the pulse-type electric fish, Pollimyrus isidori (Mormyridae) J. Comp. Physiol. 145 1982 399 403
78. A.B. Wilson, K. Noack-Kunnmann, and A. Meyer Incipient speciation in sympatric Nicaraguan crater lake cichlid fishes: sexual selection versus ecological diversification Proc. R. Soc. Lond. B Biol. Sci. 267 2000 2133 2141