The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

Molecular Ecology

Volumn 18, Issue 2, 2009, Pages 169-185

  Salzburger, Walter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Adaptive evolution; Evo devo; Evolutionary genomics; Explosive speciation; Organismal diversification; Parallel evolution

Indexed keywords

ADAPTATION; ANIMAL; CICHLID; EVOLUTION; GENETIC SELECTION; GENETICS; HISTOLOGY; QUANTITATIVE TRAIT; REVIEW; SEXUAL DEVELOPMENT; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ADAPTATION, BIOLOGICAL; ANIMALS; CICHLIDS; EVOLUTION; GENETIC SPECIATION; QUANTITATIVE TRAIT, HERITABLE; SELECTION (GENETICS); SEX CHARACTERISTICS; SPECIES SPECIFICITY;

ANIMALIA; CICHLIDAE; PISCES;

EID: 58249110498     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2008.03981.x     Document Type: Review

References (178)

1. Abzhanov A, Protas M, Grant BR, Grant PR, Tabin CJ (2004) Bmp4 and morphological variation of beaks in Darwin's finches. Science, 305, 1462 1465.
2. Abzhanov A, Kuo WP, Hartmann C, Grant BR, Grant PR, Tabin CJ (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature, 442, 563 567.
3. Abzhanov A, Extavour CG, Groover A et al 2008) Are we there yet? Tracking the development of new model systems. Trends in Genetics, 24, 353 360.
4. Albert AY, Sawaya S, Vines TH et al 2008) The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution: International Journal of Organic Evolution, 62, 76 85.
5. Albertson RC, Kocher TD (2006) Genetic and developmental basis of cichlid trophic diversity. Heredity, 97, 211 221.
6. Albertson RC, Streelman JT, Kocher TD (2003a) Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proceedings of the National Academy of Sciences, USA, 100, 5252 5257.
7. Albertson RC, Streelman JT, Kocher TD (2003b) Genetic basis of adaptive shape differences in the cichlid head. Journal of Heredity, 94, 291 301.
8. Albertson RC, Streelman JT, Kocher TD, Yelick PC (2005) Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences, USA, 102, 16287 16292.
9. Allender CJ, Seehausen O, Knight ME, Turner GF, Maclean N (2003) Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration. Proceedings of the National Academy of Sciences, USA, 100, 14074 14079.
10. Amorim MCP, Knight ME, Stratoudakis Y, Turner GF (2004) Differences in sounds made by courting males of three closely related Lake Malawi cichlid species. Journal of Fish Biology, 65, 1358 1371.
11. Arendt J, Reznick D (2008) Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends in Ecology & Evolution, 23, 26 32.
12. Arnegard ME, Markert JA, Danley PD, Stauffer JR, Ambali AJ, Kocher TD (1999) Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proceedings of the Royal Society B: Biological Sciences, 266, 119 130.
13. Aubin-Horth N, Desjardins JK, Martei YM, Balshine S, Hofmann HA (2007) Masculinized dominant females in a cooperatively breeding species. Molecular Ecology, 16, 1349 1358.
14. Baerends GP, Baerends-Van Roon JM (1950) An Introduction to the Study of the Ethology of Cichlid Fishes. E. J. Brill, Leiden, TheNetherlands.
15. Barlow GW (1976) The Midas cichlid in Nicaragua. In : Investigations of the Ichthyofauna of Nicaraguan Lakes (ed. Thorson TB pp. 333 358. School of Life Sciences, University of Nebraska, Lincoln, Nebraska.
16. Barlow GW (2000) The Cichlid Fishes Nature's Grand Experiment in Evolution. Perseus Publishing, Cambridge, Massachusetts.
17. Barluenga M, Meyer A (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? Molecular Ecology, 13, 2061 2076.
18. Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719 723.
19. Bender N, Heg D, Hamilton IM, Bachar Z, Taborsky M, Oliveira RF (2006) The relationship between social status, behaviour, growth and steroids in male helpers and breeders of a cooperatively breeding cichlid. Hormones and Behavior, 50, 173 182.
20. Bergmüller R, Heg D, Taborsky M (2005) Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proceedings of the Royal Society B: Biological Sciences, 272, 325 331.
21. Blais J, Rico C, van Oosterhout C, Cable J, Turner GF, Bernatchez L (2007) MHC adaptive divergence between closely related and sympatric African cichlids. PLoS ONE 2, e734.
22. Bolnick DI, Near TJ, Wainwrigth PC (2006) Body size divergence promotes post-zygotic reproductive isolation in centrarchids. Evoluitonary Ecology Research, 8, 908 913.
23. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecology Letters, 11, 106 115.
24. Braasch I, Salzburger W, Meyer A (2006) Asymmetric evolution in two fish specifically duplicated receptor tyrosine kinase paralogons involved in teleost coloration. Molecular Biology and Evolution, 23, 1192 1202.
25. Braasch I, Volff J-N, Schartl M (in press) The evolution of teleost pigmentation and the fish-specific genome duplication. Journal of Fish Biology.
26. Brakefield PM (2006) Evo-devo and constraints of selection. Trends in Ecology & Evolution, 21, 362 368.
27. Brandstätter A, Salzburger W, Sturmbauer C (2005) Mitochondrial phylogeny of the Cyprichromini, a lineage of open-water cichlid fishes endemic to Lake Tanganyika, East Africa. Molecular Phylogenetics and Evolution, 34, 382 391.
28. Burmeister SS (2007) Genomic responses to behavioral interactions in an African cichlid fish: mechanisms and evolutionary implications. Brain, Behavior and Evolution, 70, 247 256.
29. Burmeister SS, Jarvis ED, Fernald RD (2005) Rapid behavioral and genomic responses to social opportunity. Public Library of Science, Biology 3, e363.
30. Carleton KL, Parry JW, Bowmaker JK, Hunt DM, Seehausen O (2005) Colour vision and speciation in Lake Victoria cichlids of the genus Pundamilia. Molecular Ecology, 14, 4341 4353.
31. Carleton KL, Spady TC, Streelman JT, Kidd MR, McFarland WN, Loew ER (2008) Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biology, 6, 22.
32. Carroll SB, Grenier JK, Weatherbee SD (2005) From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design, 2nd edn. Blackwell Science, Malden, Massachusetts.
33. Clabaut C, Bunje PM, Salzburger W, Meyer A (2007) Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution: International Journal of Organic Evolution, 61, 560 578.
34. Cohen AS, Lezzar KE, Tiercelin JJ, Soreghan M (1997) New paleogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Research, 7, 107 132.
35. Coulter GW (1991) Composition of the flora and fauna. In : Lake Tanganyika and its Life (ed. Coulter GW pp. 200 274. Oxford University Press, New York.
36. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts.
37. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology, 10, 1075 1086.
38. Delvaux D (1995) Age of Lake Malawi (Nyasa) and water level fluctuations. Musée Royal Afrique Centrale, Tervuren (Belgique), Department de Geologie et Mineralogies, Rapport Annuel, 1995-1996, 99 108.
39. Dominey WJ (1984) Effects of sexual selection and life history on speciation: species flocks in African cichlids and Hawaiian Drosophila. In : Evolution of Fish Species Flocks (eds Echelle AA, Kornfield I pp. 231 250. University of Maine at Orono Press, Orono, Maine.
40. Duftner N, Sefc KM, Koblmuller S et al 2006) Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika. Molecular Ecology, 15, 2381 2395.
41. Duftner N, Sefc KM, Koblmüller S, Salzburger W, Taborsky M, Sturmbauer C (2007) Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika. Molecular Phylogenetics and Evolution, 45, 706 715.
42. Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature, 452, 169 175.
43. Fryer G (1959) The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion on the evolution of a group of rock-frequenting Cichlidae. Proceedings of the Zoological Society of London, 132, 153 281.
44. Fryer G (2004) Speciation rates in lakes and the enigma of Lake Victoria. Hydrobiologia, 519, 167 183.
45. Fryer G, Iles TD (1972) The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver & Boyd, Edinburgh, UK.
46. Fukamachi S, Shimada A, Shima A (2001) Mutations in the gene encoding B, a novel transporter protein, reduce melanin content in medaka. Nature Genetics, 28, 381 385.
47. Gavrilets S (2004) Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, New Jersey.
48. Gavrilets S, Vose A, Barluenga M, Salzburger W, Meyer A (2007) Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake. Molecular Ecology, 16, 2893 2909.
49. Genner MJ, Nichols P, Carvalho GR et al 2007a) Evolution of a cichlid fish in a Lake Malawi satellite lake. Proceedings of the Royal Society B: Biological Sciences, 274, 2249 2257.
50. Genner MJ, Seehausen O, Lunt DH et al 2007b) Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution, 24, 1269 1282.
51. Gerrard DT, Meyer A (2007) Positive selection and gene conversion in SPP120, a fertilization-related gene, during the East African cichlid fish radiation. Molecular Biology and Evolution, 24, 2286 2297.
52. Gíslason D, Ferguson MM, Skúlason S, Snorrason SS (1999) Rapid and coupled phenotypic and genetic divergence in Icelandic Arctic charr (Salvelinus alpinus). Canadian Journal of Fisheries and Aquatic Sciences, 56, 2229 2234.
53. Goldschmidt T (1991) Egg mimics in haplochromine cichlids (Pisces, Perciformes) from Lake Victoria. Ethology, 88, 177 190.
54. Goodwin NB, Balshine-Earn S, Reynolds JD (1998) Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society B: Biological Sciences, 265, 2265 2272.
55. Greenwood PH (1965) The cichlid fishes of Lake Nabugabo, Uganda. Bulletin of the British Museum of Natural History (Zoology), 12, 315 357.
56. Greenwood PH (1984) African cichlids and evolutionary theories. In : Evolution of Fish Species Flocks (eds Echelle AA, Kornfield I pp. 141 155. University of Maine at Orono Press, Orono, Maine.
57. Grosenick L, Clement TS, Fernald RD (2007) Fish can infer social rank by observation alone. Nature, 445, 429 432.
58. Haesler MP, Seehausen O (2005) Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation. Proceedings of the Royal Society B: Biological Sciences, 272, 237 245.
59. Hert E (1989) The function of egg-spots in an African mouth-brooding cichlid fish. Animal Behaviour, 37, 726 732.
60. Hoekstra HE, Coyne JA (2007) The locus of evolution: evo-devo and the genetics of adaptation. Evolution: International Journal of Organic Evolution, 61, 995 1016.
61. Hofmann HA (2003) Functional genomics of neural and behavioral plasticity. Journal of Neurobiology, 54, 272 282.
62. Hofmann HA (2006) Gonadotropin-releasing hormone signaling in behavioral plasticity. Current Opinion in Neurobiology, 16, 343 350.
63. Hulsey (2006) Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw. Proceedings of the Royal Scoeity B: Biological Sciences, 263, 669 675.
64. Hulsey CD, Roberts RJ, Lin AS, Guldberg R, Streelman JT (2008) Convergence in a mechanically complex phenotype: detecting structural adaptations for crushing in cichlid fish. International Journal of Organic Evolution, 62, 1587 1599.
65. Huysseune A (1995) Phenotypic plasticity in the lower pharyngeal jaw dentition of Astatoreochromis alluaudi (Teleostei: Cichlidae). Archives of Oral Biology, 40, 1005 1014.
66. Johnson TC, Scholz CA, Talbot MR et al 1996) Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science, 273, 1091 1093.
67. Joyce DA, Lunt DH, Bills R et al 2005) An extant cichlid fish radiation emerged in an extinct Pleistocene lake. Nature, 435, 90 95.
68. Katagiri T, Asakawa S, Minagawa S, Shimizu N, Hirono I, Aoki T (2001) Construction and characterization of BAC libraries for three fish species; rainbow trout, carp and tilapia. Animal Geneties, 32, 200 204.
69. Keenleyside MHA (1991) Parental care. In : Cichlid Fishes: Behavior, Ecology and Evolution (ed. Keenleyside MHA pp. 191 208. Chapman & Hall, London.
70. Kelsh RN, Eisen JS (2000) The zebrafish colourless gene regulates development of non-ectomesenchymal neural crest derivatives. Development, 127, 515 525.
71. Kijimoto T, Watanabe M, Fujimura K et al 2005) cimp1, a novel actin family metalloproteinase gene from East African cichlids, is differentially expressed between species during growth. Molecular Biology and Evolution, 22, 1649 1660.
72. Knight ME, Turner GF, Rico C, van Oppen MJ, Hewitt GM (1998) Microsatellite paternity analysis on captive Lake Malawi cichlids supports reproductive isolation by direct mate choice. Molecular Ecology, 7, 1605 1610.
73. Kobayashi N, Watanabe M, Kijimoto T et al 2006) magp4 gene may contribute to the diversification of cichlid morphs and their speciation. Gene, 373, 126 133.
74. Koblmüller S, Sturmbauer C, Verheyen E, Meyer A, Salzburger W (2006) Mitochondrial phylogeny and phylogeography of East African squeaker catfishes (Siluriformes: Synodontis). BMC Evolutionary Biology, 6, 49.
75. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics, 5, 288 298.
76. Kocher TD, Conroy JA, McKaye KR, Stauffer JR (1993) Similar morphologies of cichlid fish in lakes Tanganyika and Malawi are due to convergence. Molecular Phylogenetics and Evolution, 2, 158 165.
77. Konings A (1998) Tanganyikan Cichlids in Their Natural Habitat. Cichlid Press, El Paso, Texas.
78. Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annual Review of Ecology and Systematics, 31, 163 196.
79. LaBonne C, Bronner-Fraser M (1999) Molecular mechanisms of neural crest formation. Annual Review of Cell and Developmental Biology, 15, 81 112.
80. Lang M, Miyake T, Braasch I et al 2006) A BAC library of the East African haplochromine cichlid fish Astatotilapia burtoni. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution 306B, 35 44.
81. Lee BY, Lee WJ, Streelman JT et al 2005) A second generation genetic linkage map of tilapia (Oreochromis spp.). Genetics, 170, 237 244.
82. Liang H, Lin YS, Li WH (2008) Fast evolution of core promoters in primate genomes. Molecular Biology and Evolution, 25, 1239 1244.
83. Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology, 22, 425 441.
84. Loh Y-HE, Katz LS, Mims MC, Kocher TD, Yi S, Streelman JT (2008) Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology, 9, R113.
85. Maan ME, Hofker KD, van Alphen JJ, Seehausen O (2006) Sensory drive in cichlid speciation. The American Naturalist, 167, 947 954.
86. Markert JA, Arnegard ME, Danley PD, Kocher TD (1999) Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Molecular Ecology, 8, 1013 1026.
87. Mayr E (1984) Evolution of fish species flocks: a commentary. In : Evolution of Fish Species Flocks (eds Echelle AA, Kornfield I pp. 3 12. University of Maine at Orono Press, Orono, Maine.
88. McCune AR, Lovejoy NR (1998) The relative rate of sympatric and allopatric speciation in fishes. In : Endless Forms Species and Speciation (eds Howard DJ, Berlocher SH pp. 172 185. Oxford University Press, New York.
89. McKaye KR (1991) Sexual selection and the evolution of the cichlid fishes of Lake Malawi, Africa. In : Cichlid Fishes: Behavior, Ecology and Evolution (eds Keenleyside MHA pp. 241 257. Chapman & Hall, London.
90. McKinnon JS, Mori S, Blackman BK et al 2004) Evidence for ecology's role in speciation. Nature, 429, 294 298.
91. Meyer A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution, 41, 1357 1369.
92. Nagl S, Tichy H, Mayer WE, Takezaki N, Takahata N, Klein J (2000) The origin and age of haplochromine fishes in Lake Victoria, east Africa. Proceedings of the Royal Society B: Biological Sciences, 267, 1049 1061.
93. Neuhauss SC, Solnica-Krezel L, Schier AF et al 1996) Mutations affecting craniofacial development in zebrafish. Development, 123, 357 367.
94. Nishida M (1991) Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: inferences from allozyme data. Experentia, 47, 974 979.
95. van Oppen MJ, Turner GF, Rico C et al 1997) Unusually fine-scale genetic structuring found in rapidly speciating Malawi cichlid fishes. Proceedings of the Royal Society B: Biological Sciences, 264, 1803 1812.
96. van Oppen MJ, Turner GF, Rico C et al 1998) Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi. Molecular Ecology, 7, 991 1001.
97. Parichy DM, Ransom DG, Paw B, Zon LI, Johnson SL (2000) An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. Development, 127, 3031 3044.
98. Parichy DM, Rawls JF, Pratt SJ, Whitfield TT, Johnson SL (1999) Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. Development, 126, 3425 3436.
99. Parnell NF, Hulsey CD, Streelman JT (2008) Hybridization produces novelty when the mapping of form to function is many to one. BMC Evolutionary Biology, 8, 122.
100. Pereyra R, Taylor MI, Turner GF, Rico C (2004) Variation in habitat preference and population structure among three species of the Lake Malawi cichlid genus Protomelas. Molecular Ecology, 13, 2691 2697.
101. Plenderleith M, van Oosterhout C, Robinson RL, Turner GF (2005) Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish. Biological Letters, 1, 411 414.
102. Pollen AA, Dobberfuhl AP, Scace J et al 2007) Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish. Brain, Behavior and Evolution, 70, 21 39.
103. Price TD, Qvarnstrom A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society B: Biological Sciences, 270, 1433 1440.
104. Quigley IK, Manuel JL, Roberts RA et al 2005) Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus. Development, 132, 89 104.
105. Renn SC, Aubin-Horth N, Hofmann HA (2004) Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics, 5, 42.
106. Rice AN, Lobel PS (2002) Enzyme activities of pharyngeal jaw musculature in the cichlid Tramitichromis intermedius: implications for sound production in cichlid fishes. Journal of Experimental Biology, 205, 3519 3523.
107. Rice AN, Lobel PS (2003) The pharyngeal jaw apparatus of the Cichlidae and Pomacentridae: function in feeding and sound production. Reviews in Fish Biology and Fisheries, 13, 433 444.
108. Rico C, Turner GF (2002) Extreme microallopatric divergence in a cichlid species from Lake Malawi. Molecular Ecology, 11, 1585 1590.
109. Rico C, Bouteillon P, van Oppen MJ, Knight ME, Hewitt GM, Turner GF (2003) No evidence for parallel sympatric speciation in cichlid species of the genus Pseudotropheus from north-western Lake Malawi. Journal of Evolutionary Biology, 16, 37 46.
110. Rogers SM, Bernatchez L (2007) The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Molecular Biology and Evolution, 24, 1423 1438.
111. Rossiter A (1995) The cichlid fish assemblages of Lake Tanganyika: ecology, behavior and evolution of its species flocks. Advances in Ecological Research, 26, 157 252.
112. Rüber L, Adams DC (2001) Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. Journal of Evolutionary Biology, 14, 325 332.
113. Rüber L, Verheyen E, Meyer A (1999) Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proceedings of the National Academy of Sciences, USA, 96, 10230 10235.
114. Sage RD, Selander RK (1975) Trophic radiation through polymorphism in cichlid fishes. Proceedings of the National Academy of Sciences, USA, 72, 4669 4673.
115. Salzburger W (2008) To be or not to be a hamlet pair in sympatry. Molecular Ecology, 17, 1397 1399.
116. Salzburger W, Meyer A (2004) The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften, 91, 277 290.
117. Salzburger W, Baric S, Sturmbauer C (2002a) Speciation via introgressive hybridization in East African cichlids? Molecular Ecology, 11, 619 625.
118. Salzburger W, Meyer A, Baric S, Verheyen E, Sturmbauer C (2002b) Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Systematic Biology, 51, 113 135.
119. Salzburger W, Mack T, Verheyen E, Meyer A (2005) Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evolutionary Biology, 5, 17.
120. Salzburger W, Niederstätter H, Brandstätter A et al 2006) Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proceedings of the Royal Society B: Biological Sciences, 273, 257 266.
121. Salzburger W, Braasch I, Meyer A (2007) Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes. BMC Biology, 5, 51.
122. Salzburger W, Renn SC, Steinke D, Braasch I, Hofmann HA, Meyer A (2008) Annotation of expressed sequence tags for the East African cichlid fish Astatotilapia burtoni and evolutionary analyses of cichlid ORFs. BMC Genomics, 9, 96.
123. Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Molecular Ecology, 10, 1471 1488.
124. Schluter D (2000) The Ecology of Adaptive Radiation. Oxford University Press, New York.
125. Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. The American Naturalist, 140, 85 108.
126. Seehausen O (2000) Explosive speciation rates and unusual species richness in haplochromine cichlid fishes: effects of sexual selection. Advances in Ecological Research, 31, 237 274.
127. Seehausen O (2002) Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14 600 year history for its cichlid species flock. Proceedings of the Royal Society B: Biological Sciences, 269, 491 470.
128. Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198 207.
129. Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society B: Biological Sciences, 273, 1987 1998.
130. Seehausen O (2007) Chance, historical contingency and ecological determinism jointly determine the rate of adaptive radiation. Heredity, 99, 361 363.
131. Seehausen O, van Alphen JJM (1999) Can sympatric speciation by disruptive sexual selection explain rapid evolution of cichlids diversity in Lake Victoria? Ecology Letters, 2, 262 271.
132. Seehausen O, Schluter D (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proceedings of the Royal Society B: Biological Sciences, 271, 1345 1353.
133. Seehausen O, van Alphen JJM, Witte F (1997a) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808 1811.
134. Seehausen O, Witte F, Katunzi EF, Smits J, Bouton N (1997b) Patterns of the remnant cichlid fauna in Southern Lake Victoria. Conservation Biology, 11, 890 904.
135. Seehausen O, Mayhew PJ, van Alphen JJM (1999) Evolution in colour patterns in East African cichlid fish. Journal of Evolutionary Biology, 12, 514 534.
136. Seehausen O, Terai Y, Magalhaes IS et al 2008) Speciation through sensory drive in cichlid fish. Nature, 455, 620 626.
137. Sefc KM, Baric S, Salzburger W, Sturmbauer C (2007) Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. Journal of Molecular Evolution, 64, 33 49.
138. Shapiro MD, Marks ME, Peichel CL et al 2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428, 717 723.
139. Shaw PW, Turner GF, Idid MR, Robinson RL, Carvalho GR (2000) Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proceedings of the Royal Society B: Biological Sciences, 267, 2273 2280.
140. Shimeld SM, Holland PW (2000) Vertebrate innovations. Proceedings of the National Academy of Sciences, USA, 97, 4449 4452.
141. Simpson GG (1953) The Major Features of Evolution. Columbia University Press, New York.
142. van der Sluijs I, Van Dooren TJ, Hofker KD, van Alphen JJ, Stelkens RB, Seehausen O (2008) Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish. Philosophical Transactions of the Royal Society B: Biological Sciences.
143. Snoeks J (2001) Cichlid diversity, speciation and systematics: examples from the Great African Lakes. Journal of Aquariculture & Aquatic Sciences, 9, 150 166.
144. Spady TC, Seehausen O, Loew ER, Jordan RC, Kocher TD, Carleton KL (2005) Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species. Molecular Biology and Evolution, 22, 1412 1422.
145. Stager JC, Johnson TC (2008) The Late Pleistocene desiccation of Lake Victoria and the origin of its endemic biota. Hydrobiologia, 596, 5 16.
146. Stauffer JR, Gray EVS (2004) Phenotypic plasticity: its role in trophic radiation and explosive speciation in cichlids (Teleostei: Cichlidae). Animal Biology, 54, 137 158.
147. Stelkens RB, Pierotti ME, Joyce DA, Smith AM, Sluijs IV, Seehausen O (2008) Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2861 2870.
148. Streelman JT, Albertson RC (2006) Evolution of novelty in the cichlid dentition. Journal of Experimental Zoology. Part B. Molecular and Developmental Evolution, 306, 216 226.
149. Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends in Ecology & Evolution, 18, 126 131.
150. Streelman JT, Albertson RC, Kocher TD (2003a) Genome mapping of the orange blotch colour pattern in cichlid fishes. Molecular Ecology, 12, 2465 2471.
151. Streelman JT, Webb JF, Albertson RC, Kocher TD (2003b) The cusp of evolution and development: a model of cichlid tooth shape diversity. Evolution and Development, 5, 600 608.
152. Streelman JT, Peichel CL, Parichy DM (2007) Developmental genetics of adaptation in fishes: the case for novelty. Annual Review of Ecology, Evolution, and Systematics, 38, 655 681.
153. Sturmbauer C, Baric S, Salzburger W, Rüber L, Verheyen E (2001) Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Molecular Biology and Evolution, 18, 144 154.
154. Sturmbauer C, Hainz U, Baric S, Verheyen E, Salzburger W (2003) Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia, 500, 51 64.
155. Sugawara T, Terai Y, Okada N (2002) Natural selection of the rhodopsin gene during the adaptive radiation of East African Great Lakes cichlid fishes. Molecular Biology and Evolution, 19, 1807 1811.
156. Sugawara T, Terai Y, Imai H et al 2005) Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi. Proceedings of the National Academy of Sciences, USA, 102, 5448 5453.
157. Sugie A, Terai Y, Ota R, Okada N (2004) The evolution of genes for pigmentation in African cichlid fishes. Gene, 343, 337 346.
158. Taborsky M (1984) Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Animal Behaviour, 32, 1236 1252.
159. Takahashi T (2003) Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes). Ichthyological Research, 50, 367 382.
160. Taylor MI, Verheyen E (2001) Microsatellite data reveals weak population substructuring in Copadichromis sp. 'virginalis kajose', a demersal cichlid from Lake Malawi, Africa. Journal of Fish Biology, 59, 593 604.
161. Terai Y, Mayer WE, Klein J, Tichy H, Okada N (2002a) The effect of selection on a long wavelength-sensitive (LWS) opsin gene of Lake Victoria cichlid fishes. Proceedings of the National Academy of Sciences, USA, 99, 15501 15506.
162. Terai Y, Morikawa N, Kawakami K, Okada N (2002b) Accelerated evolution of the surface amino acids in the WD-repeat domain encoded by the hagoromo gene in an explosively speciated lineage of East African cichlid fishes. Molecular Biology and Evolution, 19, 574 578.
163. Terai Y, Morikawa N, Okada N (2002c) The evolution of the pro-domain of bone morphogenetic protein 4 (Bmp4) in an explosively speciated lineage of East African cichlid fishes. Molecular Biology and Evolution, 19, 1628 1632.
164. Terai Y, Morikawa N, Kawakami K, Okada N (2003) The complexity of alternative splicing of hagoromo mRNAs is increased in an explosively speciated lineage in East African cichlids. Proceedings of the National Academy of Sciences, USA, 100, 12798 12803.
165. Terai Y, Seehausen O, Sasaki T et al 2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. Public Library of Science, Biology, 4, e433.
166. Trainor BC, Hofmann HA (2006) Somatostatin regulates aggressive behavior in an African cichlid fish. Endocrinology, 147, 5119 5125.
167. Trainor BC, Hofmann HA (2007) Somatostatin and somatostatin receptor gene expression in dominant and subordinate males of an African cichlid fish. Behavioural Brain Research, 179, 314 320.
168. Turner GF (2007) Adaptive radiation of cichlid fish. Current Biology, 17, R827 R831.
169. Turner GF, Burrows MT (1995) A model of sympatric speciation by sexual selection. Proceedings of the Royal Society B: Biological Sciences, 260, 287 292.
170. Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Molecular Ecology, 10, 793 806.
171. Verheyen E, Salzburger W, Snoeks J, Meyer A (2003) Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science, 300, 325 329.
172. Watanabe M, Kobayashi N, Fujiyama A, Okada N (2003) Construction of a BAC library for Haplochromis chilotes, a cichlid fish from Lake Victoria. Genes & Genetic Systems, 78, 103 105.
173. Watanabe M, Kobayashi N, Shin-iT et al 2004) Extensive analysis of ORF sequences from two different cichlid species in Lake Victoria provides molecular evidence for a recent radiation event of the Victoria species flock: identity of EST sequences between Haplochromis chilotes and Haplochromis sp. 'Redtailsheller'. Gene, 343, 263 269.
174. West-Eberhart MJ (2003) Developmental Plasticity and Evolution. Oxford University Press, New York.
175. Wickler W (1962) 'Egg-dummies' as natural releasers in mouth-breeding cichlids. Nature, 194, 1092 1093.
176. Witte F, Goldschmidt T, Wanink J et al 1992) The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environmental Biology of Fishes, 34, 1 28.
177. Witte F, Msuku BS, Wanink JH et al 2000) Recovery of cichlid species in
178. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research, 19, 385 419.