Cichlid fishes as models of ecological diversification: patterns, mechanisms, and consequences

Hydrobiologia

Volumn 748, Issue 1, 2015, Pages 7-27

  Burress, Edward D ^a  

^a AUBURN UNIVERSITY   (United States)

Author keywords

Adaptive radiation; Cichlidae; Evolution; Niche; Speciation

Indexed keywords

EID: 84939893383     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-014-1960-z     Document Type: Review

References (151)

1. Albertson, R. C., 2008. Morphological divergence predicts habitat partitioning in a Lake Malawi cichlid species complex. Copeia 2008: 689–698.
2. Albertson, R. C. & T. D. Kocher, 2005. Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution 59: 686–690.
3. Albertson, R. C. & T. D. Kocher, 2006. Genetic and developmental basis of cichlid trophic diversity. Heredity 97: 211–221.
4. Albertson, R. C., J. T. Streelman & T. D. Kocher, 2003. Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proceedings of the National Academy of Sciences 100: 5252–5257.
5. Albertson, R. C., J. T. Streelman, T. D. Kocher & P. C. Yelick, 2005. Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences 102: 16287–16292.
6. Arbour, J. H. & H. López-Fernández, 2013. Ecological variation in South American geophagine cichlids arose during an early burst of adaptive morphological and functional evolution. Proceedings of the Royal Society B 280: 20130849.
7. Arnegard, M. E., J. Snoeks & S. A. Schaefer, 2001. New three-spotted cichlid species with hypertrophied lips (Teleostei: Cichlidae) from the deep waters of Lake Malawi/Nyasa, Africa. Copeia 2001: 705–717.
8. Barlow, G. W., 1976. The midas cichlid in Nicaragua. In Thorson, T. B. (ed.), Investigations of the Ichthyofauna of Nicaraguan Lakes. School of Life Sciences, University of Nebraska, Nebraska: 333–358.
9. Barlow, G. W. & J. W. Munsey, 1976. The red devil midas cichlid species complex in Nicaragua. In Thorson, T. B. (ed.), Investigations of the Ichthyofauna of Nicaraguan Lakes. School of Life Sciences, University of Nebraska, Lincoln, Nebraska: 359–370.
10. Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick & A. Meyer, 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439: 719–723.
11. Bootsma, H. A., R. E. Hecky, R. H. Hesslein & G. F. Turner, 1996. Food partitioning among Lake Malawi nearshore fishes as revealed by stable isotope analyses. Ecology 77: 1286–1290.
12. Burress, E. D., A. Duarte, M. M. Gangloff & L. Siefferman, 2013a. Isotopic trophic guild structure of a diverse subtropical South American fish community. Ecology of Freshwater Fish 22: 66–72.
13. Burress, E. D., A. Duarte, W. S. Serra, M. Loureiro, M. M. Gangloff & L. Siefferman, 2013b. Functional diversification within a predatory species flock. PLOS One 8: e80929.
14. Burress, E. D., A. Duarte, W. S. Serra, M. M. Gangloff & L. Siefferman, 2013c. Species-specific ontogenetic diet shifts among Neotropical Crenicichla: using stable isotopes and tissue stoichiometry. Journal of Fish Biology 82: 1904–1915.
15. Campbell, L. M., R. E. Hecky & S. B. Wandera, 2003. Stable isotope analyses of food web structure and fish diet in Napoleon and Winam Gulfs, Lake Victoria, East Africa. Journal of Great Lakes Research 29: 243–257.
16. Casciotta, J. R. & G. Arratia, 1993. Jaws and teeth of American cichlids (Pisces: Labroidei). Journal of Morphology 217: 1–36.
17. Clabaut, C., P. M. E. Bunje, W. Salzburger & A. Meyer, 2007. Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61: 560–578.
18. Cochran-Biederman, J. L. & K. O. Winemiller, 2013. Relationships among habitat, ecomorphology and diets of cichlids in the Bladen River, Belize. Environmental Biology of Fish 88: 143–152.
19. Collar, D. C., B. C. O’Meara, P. C. Wainwright & T. J. Near, 2009. Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution 63: 1557–1573.
20. Colombo, M., E. T. Diepeveen, M. Muschick, M. E. Santos, A. Indermaur, N. Bioileau, M. Barluenga & W. Salzburger, 2012. The ecological and genetic basis of convergent thick-lipped phenotypes in cichlid fishes. Molecular Ecology 22: 670–684.
21. Connell, J. H., 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35: 131–138.
22. Cooper, W. J., K. Parsons, A. McIntyre, B. Kern, A. McGee-Moore & R. C. Albertson, 2010. Bentho-pelagic divergence was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLOS One 5: e9551.
23. Crampton, W. G. R., 2008. Ecology and life history of an Amazon floodplain cichlid: the discus fish Symphysodon (Perciformes: Cichlidae). Neotropical Ichthyology 6: 599–612.
24. Day, J. J., J. A. Cotton & T. G. Barraclough, 2008. Tempo and mode of diversification of Lake Tanganyika cichlid fishes. PLOS One 3: e1730.
25. de Mérona, B. & J. Rankin de Mérona, 2004. Food resource partitioning in a fish community of the central Amazon floodplain. Neotropical Ichthyology 2: 75–84.
26. Diehl, S., 2003. The evolution and maintenance of omnivory: dynamic constraints and the role of food quality. Ecology 84: 2557–2567.
27. Drucker, E. G. & J. S. Jensen, 1991. Functional analysis of a specialized prey processing behavior: winnowing by surfperches (Teleostei: Embiotocidae). Journal of Morphology 210: 267–287.
28. Duftner, N., S. Koblmüller & C. Sturmbauer, 2005. Evolutionary relationships of the Limnochromini, a tribe of benthic deepwater cichlid fish endemic to Lake Tanganyika, East Africa. Journal of Molecular Evolution 60: 277–289.
29. Duponchelle, F., A. J. Ribbink, A. Msukwa, J. Mafuka, D. Mandere & H. Bootsma, 2005. Food partitioning within the species-rich benthic fish community of Lake Malawi, East Africa. Canadian Journal of Fisheries and Aquatic Sciences 62: 1651–1664.
30. Elmer, K. R. & A. Meyer, 2011. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends in Ecology and Evolution 26: 298–306.
31. Elmer, K. R., T. K. Lehtonen, A. F. Kautt, C. Harrod & A. Meyer, 2010a. Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times. BMC Biology 8: 60.
32. Elmer, K. R., H. Kusche, T. K. Lehtonen & A. Meyer, 2010b. Local variation and parallel evolution: morphological and genetic diversity across a species complex of Neotropical crater lake cichlid fishes. Philosophical Transactions of the Royal Society B 365: 1763–1782.
33. Fan, S., K. R. Elmer & A. Meyer, 2012. Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philosophical Transactions of the Royal Society B 367: 385–394.
34. Franchini, P., C. Fruciano, M. L. Spreitzer, J. C. Jones, K. R. Elmer, F. Henning & A. Meyer, 2013. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Molecular Ecology 23: 1828–1845.
35. Franchini, P., C. Fruciano, T. Frickey, J. C. Jones & A. Meyer, 2014. The gut microbial community of midas cichlid fish in repeatedly evolved limnetic–benthic species pairs. PLOS One 9: e95027.
36. Fraser, G. J., C. D. Hulsey, R. F. Bloomquist, K. Uyesugi, N. R. Manley & J. T. Streelman, 2009. An ancient gene network is co-opted for teeth on old and new jaws. PLOS Biology 7: e1000031.
37. Fraser, G. J., R. F. Bloomquist & J. T. Streelman, 2013. Common developmental pathways link tooth shape to regeneration. Developmental Biology 377: 399–414.
38. Friedman, M., B. P. Keck, A. Dornburg, R. I. Eytan, C. H. Martin, C. D. Hulsey, P. C. Wainwright & T. J. Near, 2013. Molecular and fossil evidence place the origin of cichlid fishes long after Gondwanan rifting. Proceedings of the Royal Society B 280: 20131733.
39. Fryer, G., 1959. The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with special reference to the fishes, and a discussion on the evolution of rock-frequenting Cichlidae. Proceedings of the Zoological Society of London 132: 153–281.
40. Fryer, G. & T. D. Iles, 1972. The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver & Boyd, Edinburgh.
41. Geiger, M. F., J. K. McCrary & U. K. Schliewen, 2013. Crater Lake Apoyo revisited—population genetics of an emerging species flock. PLOS One 8: e74901.
42. Genner, M. J., G. F. Turner & S. J. Hawkins, 1999. Foraging of rocky habitat cichlid fishes in Lake Malawi: coexistence through niche partitioning? Oecologia 121: 283–292.
43. Gerking, S. D., 1994. Feeding Ecology of Fish. Academic Press, London.
44. Goldschmidt, T., F. Witte & J. de Visser, 1990. Ecological segregation in zooplanktivorous Haplochromine species (Pisces: Cichlidae) from Lake Victoria. Oikos 58: 343–355.
45. González-Bergonzoni, M., T. A. Meerhoff, F. Teizeira-de Mello, A. Baattrup-Pedersen & E. Jeppesen, 2012. Meta-analysis shows a consistent and strong latitudinal pattern in fish omnivory across ecosystems. Ecosystems 15: 492–503.
46. Greenwood, P. H., 1974. The cichlid fishes of Lake Victoria East Africa: the biology and evolution of a species flock. Bulletin of the British Museum for Natural History Supplementary 6: 1–134.
47. Gunter, H. M., S. Fan, F. Xiong, P. Franchini, C. Fruciano & A. Meyer, 2013. Shaping development through mechanical strain: the transcriptional basis of diet-induced phenotypic plasticity in cichlid fish. Molecular Ecology 22: 4516–4531.
48. Gysels, E., L. Janssens de Bisthoven, L. de Vos & F. Ollevier, 1997. Food and habitat of four Xenotilapia species (Teleostei, Cichlidae) in a sandy bay of northern Lake Tanganyika (Burundi). Journal of Fish Biology 50: 254–266.
49. Hellig, C. J., M. Kerschbaumer, K. M. Sefc & S. Koblmüller, 2010. Allometric shape change of the lower pharyngeal jaw correlates with a dietary shift to piscivory in a cichlid fish. Naturwissenschaften 97: 663–672.
50. Higham, T. E., C. D. Hulsey, O. Rícan & A. M. Carroll, 2006. Feeding with speed: prey capture evolution in cichlids. Journal of Evolutionary Biology 20: 70–78.
51. Hori, M., 1993. Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260: 216–219.
52. Hu, Y. & R. C. Albertson. 2014. Hedgehog signaling mediates adaptive variation in a dynamic functional system in the cichlid feeding apparatus. Proceedings of the National Academy of Sciences. doi: 10.1073/pnas.1323154111.
53. Hu, Y., K. J. Parsons & R. C. Albertson, 2013. Evolvability of the cichlid jaw: new tools provide insights into the genetic basis of phenotypic integration. Evolutionary Biology 41: 145–153.
54. Hulsey, C. D., 2006. Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw. Proceedings of the Royal Society B 273: 669–675.
55. Hulsey, C. D. & F. J. G. De León, 2005. Cichlid jaw mechanics: linking morphology to feeding specialization. Functional Ecology 19: 487–494.
56. Hulsey, C. D., J. Marks, D. A. Hendrickson, C. A. Williamson, A. E. Cohen & M. J. Stephens, 2006. Feeding specialization in Herichthys minckleyi: a trophically polymorphic fish. Journal of Fish Biology 68: 1399–1410.
57. Hulsey, C. D., R. J. Roberts, A. S. P. Lin, R. Guldberg & T. J. Streelman, 2008. Convergence in a mechanically complex phenotype: detecting structural adaptations for crushing in cichlid fish. Evolution 62: 1587–1599.
58. Hulsey, C. D., M. C. Mims, N. F. Parnell & J. T. Streelman, 2010. Comparative rates of lower jaw diversification in cichlid adaptive radiations. Journal of Evolutionary Biology 23: 1456–1467.
59. Hulsey, C. D., R. J. Roberts, Y. H. E. Loh, M. F. Rupp & J. T. Streelman, 2013. Lake Malawi cichlid evolution along a benthic/limnetic axis. Ecology and Evolution 3: 2262–2272.
60. Huysseune, A., 1995. Phenotypic plasticity in the lower pharyngeal jaw dentition of Astatoreochromis alluaudi (Teleostei: Cichlidae). Archives of Oral Biology 40: 1005–1014.
61. Ilves, K. L. & H. López-Fernández, 2014. A targeted next-generation sequencing toolkit for exon-based cichlid phylogenomics. Molecular Ecology Resources. doi: 10.1111/1755-0998.12222.
62. Irschick, D. J., R. C. Albertson, R. Brennan, J. Podos, N. A. Johnson, S. Patek & E. Dumont, 2013. Evo-devo beyond morphology: from genes to resource use. Trends in Ecology and Evolution 28: 267–273.
63. Jepsen, D. B. & K. O. Winemiller, 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos 96: 46–55.
64. Keller, I., C. E. Wagner, L. Gueter, S. Mwaiko, O. M. Selz, A. Sizasundar, S. Wittwer & O. Seehausen, 2012. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Molecular Ecology 22: 2848–2863.
65. Kidd, M. R., C. E. Kidd & T. D. Kocher, 2006. Axes of differentiation in the bower-building cichlids of Lake Malawi. Molecular Ecology 15: 459–478.
66. Koblmüller, S., N. Duftner, K. M. Sefc, M. Aibara, M. Stipacek, M. Blanc, B. Egger & C. Sturmbauer, 2007. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika—the result of repeated introgressive hybridization. BMC Evolutionary Biology 7: 7.
67. Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.
68. Konan, K. J., B. C. Atse & N. J. Kouassi, 2011. Food and feeding ecology of Tylochromis jentinki (Teleostei: Cichlidae) in Ebrié Lagoon, Ivory Coast, with emphasis on spatial, size and temporal variation in fish diet. African Journal of Aquatic Sciences 36: 75–82.
69. Konings, A., 1998. Tanganyikan Cichlids in Their Natural Habitat. Cichlid Press, El Paso.
70. Kornfield, I. & J. N. Taylor, 1983. A new species of polymorphic fish, Cichlasoma minckleyi, from Cuatro Cienegas, Mexico (Teleostei: Cichlidae). Proceedings of the Biological Society of Washington 96: 253–269.
71. Kullander, S., M. Norén, G. B. Friöriksson & C. A. Santos de Lucena, 2010. Phylogenetic relationships of species of Crenicichla (Teleostei: Cichlidae) from southern South America based on the mitochondrial cytochrome b gene. Journal of Zoological Systematics and Evolutionary Research 48: 248–253.
72. Kusche, H., H. J. Lee & A. Meyer, 2012. Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all. Proceedings of the Royal Society B 279: 4715–4723.
73. Kusche, H., H. Recknagel, K. B. Elmer & A. Meyer, 2014. Crater lake cichlids individually specialize along the benthic–limnetic axis. Ecology and Evolution 4: 1127–1139.
74. León-Romero, Y., O. Mejía & E. Soto-Galera, 2012. DNA barcoding reveals taxonomic conflicts in the Herichthys bartoni species group (Pisces: Cichlidae). Molecular Ecology Resources 12: 1021–1026.
75. Liem, K. F., 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22: 425–441.
76. Liem, K. F., 1980. Adaptive significance of intraspecific and interspecific differences in the feeding repertoires of cichlid fishes. American Zoologist 20: 295–314.
77. López-Fernández, H., K. O. Winemiller & R. L. Honeycutt, 2010. Multilocus phylogeny and rapid radiations in neotropical cichlid fishes (Perciformes: Cichlidae: Cichlinae). Molecular Phylogenetics and Evolution 55: 1070–1086.
78. López-Fernández, H., K. O. Winemiller, C. Montaña & R. L. Honeycutt, 2012. Diet–morphology correlations in the radiation of South American Geophagine cichlids (Perciformes: Cichlidae: Cichlinae). PLOS One 7(4): e33997.
79. López-Fernández, H., J. H. Arbour, K. O. Winemiller & R. L. Honeycutt, 2013. Testing for ancient adaptive radiations in neotropical cichlid fishes. Evolution 67: 1321–1337.
80. López-Fernández, H., J. Arbour, S. Willis, C. Watkins, R. L. Honeycutt & K. O. Winemiller, 2014. Morphology and efficiency of a specialized foraging behavior, sediment sifting, in neotropical cichlid fishes. PLOS One 9(3): e89832.
81. Losos, J. B., 2011. Convergence, adaptation, and constraint. Evolution 65: 1827–1840.
82. Lucena, C. A. S. & S. O. Kullander, 1992. The Crenicichla (Teleostei: Cichlidae) species of the Uruguai River drainage in Brazil. Ichthyological Explorations of Freshwaters 3: 97–160.
83. Machado-Schiaffino, G., F. Henning & A. Meyer, 2014. Species-specific differences in adaptive phenotypic plasticity in an ecologically relevant trophic trait: hypertrophic lips in Midas cichlid fishes. Evolution. doi:10.1111/evo.12367.
84. Mahler, D. L., L. J. Revell, R. E. Glor & J. B. Losos, 2010. Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean anoles. Evolution 64: 2731–2745.
85. Mallet, J., 2007. Hybrid speciation. Nature 446: 279–283.
86. Manousaki, T., P. M. Hull, H. Kusche, G. Machado-Schiaffino, P. Franchini, C. Harrod, K. R. Elmer & A. Meyer, 2013. Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua. Molecular Ecology 22: 650–669.
87. Martin, C. H., 2012. Weak disruptive selection and incomplete phenotypic divergence in two classic examples of sympatric speciation: Cameroon Crater Lake cichlids. The American Naturalist 180: 90–109.
88. McMahan, C. D., A. D. Geheber & K. R. Piller, 2010. Molecular systematics of the enigmatic Middle American genus Vieja (Teleostei: Cichlidae). Molecular Phylogenetics and Evolution 57: 1293–1300.
89. McMahan, C. D., P. Chakrabarty, J. S. Sparks, W. L. Smith & M. P. Davis, 2013. Temporal patterns of diversification across global cichlid biodiversity (Acanthomorpha: Cichlidae). PLOS One 8(8): e71162.
90. Meyer, A., 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357–1369.
91. Meyer, A., 1989. Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fishes, Cichlasoma citrinellum. Oecologia 80: 431–436.
92. Mittelbach, G. G., 1984. Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65: 499–513.
93. Mittelbach, G. G., 1988. Competition among refuging sunfishes and effects of fish density on littoral zone invertebrates. Ecology 69: 614–623.
94. Montaña, C. G. & K. O. Winemiller, 2009. Comparative feeding ecology and habitats use of Crenicichla species (Perciformes: Cichlidae) in a Venezuelan floodplain river. Neotropical Ichthyology 7: 267–274.
95. Montaña, C. G. & K. O. Winemiller, 2013. Evolutionary convergence in neotropical cichlids and nearctic centrarchids: evidence from morphology, diet, and stable isotope analysis. Biological Journal of the Linnean Society 109: 146–164.
96. Muschick, M., A. Indermaur & W. Salzburger, 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 1–7.
97. Near, T. J., A. Dornburg, R. I. Eytan, B. P. Keck, W. L. Smith, K. L. Kuhn, J. A. Moore, S. A. Price, F. T. Burbrink, M. Friendman & P. C. Wainwright, 2013. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proceedings of the National Academy of Sciences 110: 12738–12743.
98. Nosil, P., 2012. Ecological Speciation. Oxford University Press, New York.
99. Oliver, M. K. & M. E. Arnegard, 2010. A new genus for Melanochromis labrosus, a problematic Lake Malawi cichlid with hypertrophied lips (Teleostei: Cichlidae). Ichthyological Exploration of Freshwaters 21: 209–232.
100. Parnell, N. F., C. D. Hulsey & J. T. Streelman, 2008. Hybridization produces novelty when mapping of form to function is many to one. BMC Evolutionary Biology 8: 122.
101. Parnell, N. F., C. D. Hulsey & J. T. Streelman, 2012. The genetic basis of a complex functional system. Evolution 66: 3352–3366.
102. Parsons, K. J., W. J. Cooper & R. C. Albertson, 2011. Modularity of the oral jaws is linked to repeated changes in the cranial shape of African cichlids. International Journal of Evolutionary Biology. doi: 10.4061/2011/641501.
103. Parsons, K. J., A. T. Taylor, K. E. Powder & R. C. Albsertson, 2014. Wnt signaling underlies the evolution of new phenotypes and craniofacial variability in Lake Malawi cichlids. Nature Communications 5. doi: 10.1038/ncomms4629.
104. Parsons, K. J. & R. C. Albertson, 2009. Roles for BMP4 and CAM1 in shaping the jaw: evo-devo and beyond. Annual Review of Genetics 43: 369–388.
105. Parsons, K. J., Y. H. Son & R. C. Albertson, 2011b. Hybridization promotes evolvability in African cichlids: connections between transgressive segregation and phenotypic integration. Evolutionary Biology 38: 306–315.
106. Pfennig, D. W., M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting & A. P. Moczek, 2010. Phenotypic plasticity’s impacts on diversification and speciation. Trends in Ecology and Evolution 25: 459–467.
107. Piálek, L., O. Rícan, J. Casciotta, A. Almirón & J. Zrzavy, 2012. Multilocus phylogeny of Crenicichla (Teleostei: Cichlidae), with biogeography of the C. lacustris group: species flocks as a model for sympatric speciation in rivers. Molecular Phylogenetics and Evolution 62: 46–61.
108. Rabosky, D. L., F. Santini, J. Eastman, S. A. Smith, B. Sidlauskas, J. Chang & M. E. Alfaro, 2013. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications 4: 1958.
109. Recknagel, H., K. R. Elmer & A. Meyer, 2013. A hybrid genetic linkage map of two ecologically and morphologically divergence midas cichlid fishes (Amphilophus spp.) obtained by massively parallel DNA sequencing (ddRADseq). Genes, Genomes, Genetics 3: 65–74.
110. Recknagel, H., K. R. Elmer & A. Meyer, 2014. Crater lake habitat predicts morphological diversity in adaptive radiations of cichlid fishes. Evolution doi: 10.1111/evo.12412.
111. Reinthal, P. N., 1989. The gross intestine morphology of a group of rock-dwelling cichlid fishes (Pisces, Teleostei) from Lake Malawi. Netherlands Journal of Zoology 39: 208–225.
112. Reis, R. E. & L. R. Malabarba, 1988. Revision of the neotropical cichlid genus Gymnogeophagus Ribeiro, 1918, with descriptions of two new species (Pisces, Perciformes). Revista Brasileira de Zoologia 4: 259–305.
113. Rícan, O., L. Piálek, R. Zardoya, I. Doadrico & J. Zrzavy, 2013. Biogeography of the Mesoamerican Cichlidae (Teleostei: Heroini): colonization through the GAARlandia land bridge and early diversification. Journal of Biogeography 40: 579–593.
114. Roberts, R. B., Y. Hu, R. C. Albsertson & T. D. Kocher, 2011. Craniofacial divergence and ongoing adaptation via the hedgehog pathway. Proceedings of the National Academy of Sciences 108: 13194–13199.
115. Rüber, L., E. Verheyen & A. Meyer, 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.
116. Rudnick, D. & V. Resh, 2005. Stable isotope, mesocosm and gut contents analysis demonstrate trophic differences in two invasive decapod crustacea. Freshwater Biology 50: 1323–1336.
117. Sage, R. D. & R. K. Selander, 1975. Trophic radiation through polymorphism in cichlid fishes. Proceedings of the National Academy of Sciences USA 72: 4669–4673.
118. Salzburger, W., S. Baric & C. Sturmbauer, 2002. Speciation via introgressive hybridization in East African cichlids? Molecular Ecology 11: 619–625.
119. Salzburger, W., T. Mack, E. Verheyen & A. Meyer, 2005. Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evolutionary Biology 5: 17.
120. Sazima, I., 1986. Similarities in feeding behavior between some marine and freshwater fishes in two tropical communities. Journal of Fish Biology 29: 53–65.
121. Schliewen, U., K. Rassmann, M. Markmann, J. Markert, T. Kocher & D. Tautz, 2001. Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Molecular Ecology 10: 1471–1488.
122. Seehausen, O., 1996. Lake Victoria Rock Cichlids: Taxonomy, Ecology, and Distribution. Verduijn Cichlids, Zevenhuizen, The Netherlands.
123. Seehausen, O., 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198–207.
124. Seehausen, O. & N. Bouton, 1997. Microdistribution and fluctuations in niche overlap in a rocky shore cichlid community in Lake Victoria. Ecology of Freshwater Fish 6: 161–173.
125. Seehausen, O. & D. Schluter, 2004. Male–male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proceedings of the Royal Society B 271: 1345–1553.
126. Selz, O. M., K. Lucek, K. A. Young & O. Seehausen, 2014a. Relaxed train covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations. Evolutionary Biology 27: 11–24.
127. Selz, O. M., R. Thommen, M. E. Maan & O. Seehausen, 2014b. Behavioral isolation may facilitate homoploid hybrid speciation in cichlid fish. Evolutionary Biology 27: 275–289.
128. Smits, J. D., F. Witte & F. G. Van Veen, 1996. Functional changes in the anatomy of the pharyngeal jaw apparatus of Astatoreochromis alluaudi (Pisces, Cichlidae), and their effects on adjacent structures. Biological Journal of the Linnean Society 59: 389–409.
129. Stauffer, J. R. & E. V. S. Gray, 2004. Phenotypic plasticity: its role in trophic radiation and explosive speciation in cichlids (Teleostei: Cichlidae). Animal Biology 54: 137–158.
130. Stauffer, J. R. & I. Posner, 2006. An investigation of the utility of feeding angles among Lake Malawi rock-dwelling cichlids (Teleostei: Cichlidae). Copeia 2006: 289–292.
131. Streelman, J. T. & R. C. Albertson, 2006. Evolution of novelty in the cichlid dentition. Journal of Experimental Zoology 306: 216–226.
132. Streelman, J. T., J. F. Webb, R. C. Albertson & T. D. Kocher, 2003. The cusp of evolution and development: a model of cichlid tooth shape diversity. Evolution & Development 5: 600–608.
133. Sturmbauer, C., W. Mark & R. Dallinger, 1992. Ecophysiology of aufwuchs-eating cichlids in Lake Tanganyika: niche separation by trophic specialization. Environmental Biology of Fishes 35: 283–290.
134. Sturmbauer, C., M. Husemann & P. D. Danley, 2011. Explosive speciation and adaptive radiation of East African cichlid fishes. In Zachos, F. E. & J. C. Habel (eds), Biodiversity Hotspots. Springer, Berlin: 333–362.
135. Takahashi, R., K. Watanabe, M. Nishida & M. Hori, 2007. Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach. BMC Evolutionary Biology 7: 195.
136. Terai, O. Seehausen, T. Sasaki, K. Takahashi, S. Mizoiri, T. Sugawara, T. Sato, M. Watanabe, N. Konijnendijk, H. D. J. Mrosso, H. Tachida, H. Imai, Y. Shichida & N. Okada, 2006. Divergent selection on Opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biology 4: e433.
137. Wagner, C. E., P. B. McIntyre, K. S. Buels, D. M. Gilbert & E. Michel, 2009. Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Functional Ecology 23: 1122–1131.
138. Wagner, C. E., L. J. Harmon & O. Seehausen, 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487: 366–370.
139. Wagner, C. E., I. Keller, S. Wittwer, O. M. Selz, S. Mwaiko, L. Greuter, A. Sivasundar & O. Seehausen, 2013. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Molecular Ecology 22: 787–798.
140. Wainwright, P. C., L. A. Ferry-Graham, T. B. Waltzek, A. M. Carroll, C. D. Hulsey & J. R. Grubich, 2001. Evaluating the use of ram and suction during prey capture by cichlid fishes. The Journal of Experimental Biology 204: 3039–3051.
141. Wainwright, P. C., W. L. Smith, S. A. Price, K. L. Tang, J. S. Sparks, L. A. Ferry, K. L. Kuhn, R. I. Eytan & T. J. Near, 2012. The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Systematic Biology 61: 1001–1027.
142. Waltrek, T. B. & P. C. Wainwright, 2003. Functional morphology of extreme jaw protrusion in neotropical cichlids. Journal of Morphology 257: 96–106.
143. Willis, S. C., J. Macrander, I. P. Farias & G. Orti, 2012. Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evolutionary Biology 12: 96.
144. Wimberger, P. H., 1991. Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45: 1545–1563.
145. Winemiller, K. O., 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environmental Biology of Fishes 26: 177–199.
146. Winemiller, K. O., L. C. Kelso-Winemiller & A. L. Brenkert, 1995. Ecomorphological diversification and convergence in fluvial cichlid fishes. Environmental Biology of Fishes 44: 235–261.
147. Winemiller, K. O., D. J. Hoeinghaus, A. A. Pease, P. C. Esselman, R. L. Honeycutt, D. Gbanaador, E. Carrera & J. Payne, 2011. Stable isotope analysis reveals food web structure and watershed impacts along the fluvial gradient of a Mesoamerican coastal river. River Research and Applications 27: 791–803.
148. Winkelmann, K., M. J. Genner, T. Takahsashi & L. Rüber, 2014. Competition-driven speciation in cichlid fish. Nature Communications 5: 3412.
149. Yamaoka, K., 1997. Trophic ecomorphology of Tanganyikan cichlids. In Kawanabe, H., M. Hori & M. Nagoshi (eds), Fish Communities in Lake Tanganyika. Kyoto University Press, Kyoto: 27–56.
150. Yoder, J. B., E. Clancey, S. D. Roches, J. M. Eastman, L. Gentry, W. Godsoe, T. J. Hagey, D. Jochimsen, B. P. Oswald, J. Robertson, B. A. J. Sarver, J. J. Schenk, S. F. Spear & L. J. Harmon, 2010. Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology 23: 1581–1596.
151. Young, K. A., J. Snoeks & O. Seehausen, 2009. Morphological diversity and the roles of contingency, chance and determinisms in African cichlid radiations. PLOS One 4: e4740.