Hydrobiologia

, Volume 748, Issue 1, pp 7–27

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

ADVANCES IN CICHLID RESEARCH Review Paper

Abstract

Cichlid fishes are hypothesized to encompass several independent adaptive radiations that display increased diversification rates and impressive ecological heterogeneity. Here, I review major ecological patterns associated with the evolutionary history of cichlids, with particular focus on comparison of Afrotropical and Neotropical lineages. Specifically, I present major patterns of ecological diversification, potential mechanisms that may promote ecological diversification, and possible consequences of ecological diversification. Evolutionary convergence and specialization of ecological (e.g., diet), behavioral (e.g., benthic sifting), and morphological traits (e.g., oral dentition) characterize adaptive patterns that transcend continents. Craniofacial mechanics, the pharyngeal jaw apparatus, phenotypic plasticity, and hybridization may have facilitated diversification of cichlid fishes by generating functional, morphological, and/or genetic diversity. The benthic–pelagic axis has been an important source of divergence during adaptive radiation. Additionally, there are several discrepancies between Afrotropical and Neotropical lineages, such as the relative frequency of herbivorous species, the importance of hybridization in generating diversity, the relative frequency of dentition types, and relationships between dental organization and ecological function. Emphasis on contrasts between Neotropical and Afrotropical lineages improves characterization of patterns at a broader level of organization and indicates that the genetic basis, functional capacity, and ecological opportunity for many traits may be conserved across lineages.

Keywords

Adaptive radiation Cichlidae Evolution Niche Speciation 

References

  1. Albertson, R. C., 2008. Morphological divergence predicts habitat partitioning in a Lake Malawi cichlid species complex. Copeia 2008: 689–698.Google Scholar
  2. Albertson, R. C. & T. D. Kocher, 2005. Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution 59: 686–690.PubMedGoogle Scholar
  3. Albertson, R. C. & T. D. Kocher, 2006. Genetic and developmental basis of cichlid trophic diversity. Heredity 97: 211–221.PubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  16. Casciotta, J. R. & G. Arratia, 1993. Jaws and teeth of American cichlids (Pisces: Labroidei). Journal of Morphology 217: 1–36.Google Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  21. Connell, J. H., 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35: 131–138.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  26. Diehl, S., 2003. The evolution and maintenance of omnivory: dynamic constraints and the role of food quality. Ecology 84: 2557–2567.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedCentralGoogle Scholar
  37. Fraser, G. J., R. F. Bloomquist & J. T. Streelman, 2013. Common developmental pathways link tooth shape to regeneration. Developmental Biology 377: 399–414.PubMedCentralPubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  40. Fryer, G. & T. D. Iles, 1972. The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver & Boyd, Edinburgh.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  43. Gerking, S. D., 1994. Feeding Ecology of Fish. Academic Press, London.Google Scholar
  44. Goldschmidt, T., F. Witte & J. de Visser, 1990. Ecological segregation in zooplanktivorous Haplochromine species (Pisces: Cichlidae) from Lake Victoria. Oikos 58: 343–355.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  51. Hori, M., 1993. Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260: 216–219.PubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  55. Hulsey, C. D. & F. J. G. De León, 2005. Cichlid jaw mechanics: linking morphology to feeding specialization. Functional Ecology 19: 487–494.Google Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  60. Huysseune, A., 1995. Phenotypic plasticity in the lower pharyngeal jaw dentition of Astatoreochromis alluaudi (Teleostei: Cichlidae). Archives of Oral Biology 40: 1005–1014.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  63. Jepsen, D. B. & K. O. Winemiller, 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos 96: 46–55.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  67. Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.PubMedGoogle Scholar
  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.Google Scholar
  69. Konings, A., 1998. Tanganyikan Cichlids in Their Natural Habitat. Cichlid Press, El Paso.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedGoogle Scholar
  75. Liem, K. F., 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Systematic Zoology 22: 425–441.Google Scholar
  76. Liem, K. F., 1980. Adaptive significance of intraspecific and interspecific differences in the feeding repertoires of cichlid fishes. American Zoologist 20: 295–314.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  81. Losos, J. B., 2011. Convergence, adaptation, and constraint. Evolution 65: 1827–1840.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  85. Mallet, J., 2007. Hybrid speciation. Nature 446: 279–283.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  92. Mittelbach, G. G., 1984. Predation and resource partitioning in two sunfishes (Centrarchidae). Ecology 65: 499–513.Google Scholar
  93. Mittelbach, G. G., 1988. Competition among refuging sunfishes and effects of fish density on littoral zone invertebrates. Ecology 69: 614–623.Google Scholar
  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.Google Scholar
  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.Google Scholar
  96. Muschick, M., A. Indermaur & W. Salzburger, 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 1–7.Google Scholar
  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.Google Scholar
  98. Nosil, P., 2012. Ecological Speciation. Oxford University Press, New York.Google Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  101. Parnell, N. F., C. D. Hulsey & J. T. Streelman, 2012. The genetic basis of a complex functional system. Evolution 66: 3352–3366.PubMedCentralPubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  118. Salzburger, W., S. Baric & C. Sturmbauer, 2002. Speciation via introgressive hybridization in East African cichlids? Molecular Ecology 11: 619–625.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  122. Seehausen, O., 1996. Lake Victoria Rock Cichlids: Taxonomy, Ecology, and Distribution. Verduijn Cichlids, Zevenhuizen, The Netherlands.Google Scholar
  123. Seehausen, O., 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198–207.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  131. Streelman, J. T. & R. C. Albertson, 2006. Evolution of novelty in the cichlid dentition. Journal of Experimental Zoology 306: 216–226.PubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar
  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.Google Scholar
  138. Wagner, C. E., L. J. Harmon & O. Seehausen, 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487: 366–370.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  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.PubMedGoogle Scholar
  142. Waltrek, T. B. & P. C. Wainwright, 2003. Functional morphology of extreme jaw protrusion in neotropical cichlids. Journal of Morphology 257: 96–106.Google Scholar
  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.PubMedCentralPubMedGoogle Scholar
  144. Wimberger, P. H., 1991. Plasticity of jaw and skull morphology in the neotropical cichlids Geophagus brasiliensis and G. steindachneri. Evolution 45: 1545–1563.Google Scholar
  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.Google Scholar
  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.Google Scholar
  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.Google Scholar
  148. Winkelmann, K., M. J. Genner, T. Takahsashi & L. Rüber, 2014. Competition-driven speciation in cichlid fish. Nature Communications 5: 3412.PubMedGoogle Scholar
  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.Google Scholar
  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.PubMedGoogle Scholar
  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.PubMedCentralPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of Biological SciencesAuburn University Museum of Natural History, Auburn UniversityAuburnUSA

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