Table of Contents
International Journal of Evolutionary Biology
Volume 2011 (2011), Article ID 290245, 8 pages
http://dx.doi.org/10.4061/2011/290245
Review Article

The Utility of Geometric Morphometrics to Elucidate Pathways of Cichlid Fish Evolution

Department of Zoology, Karl-Franzens University of Graz, Universitätsplatz 2, 8010 Graz, Austria

Received 22 December 2010; Accepted 29 March 2011

Academic Editor: Tetsumi Takahashi

Copyright © 2011 Michaela Kerschbaumer and Christian Sturmbauer. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. F. Turner, O. Seehausen, M. E. Knight, C. Allender, and R. L. Robinson, “How many species of cichlid fishes are there in African lakes?” Molecular Ecology, vol. 10, no. 3, pp. 793–806, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Koblmüller, K. M. Sefc, and C. Sturmbauer, “The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics,” Hydrobiologia, vol. 615, no. 1, pp. 5–20, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. G. A. Boulenger, Catalogue of the Fresh-Water Fishes of Africa in the British Museum (Natural History), vol. 3, British Museum (Natural History), London, UK, 1898.
  4. G. Fryer and T. D. Iles, The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution, Oliver & Boyd, Edinbourgh, UK, 1972.
  5. P. H. Greenwood, “Morphology, endemism and speciation in African cichlid fishes,” Verhandlungen der Deutschen Zoologischen Gesellschaft, vol. 66, pp. 115–124, 1973. View at Google Scholar
  6. P. H. Greenwood, “The cichlid fishes of Lake Victoria, East Africa: the biology and evolution of a species flock,” in Zoology, Bulletin of the British Museum (Natural History), supplement 6, Natural History Museum, London, UK, 1974. View at Google Scholar
  7. P. H. Greenwood, “What is a species flock?” in Evolution of Fish Species Flocks, A. A. Echelle and I. Kornfield, Eds., pp. 13–19, University of Maine at Orono Press, 1984. View at Google Scholar
  8. P. H. Greenwood, “African cichlids and evolutionary theories,” in Evolution of Fish Species Flocks, A. A. Echelle and I. Kornfield, Eds., pp. 141–155, University of Maine at Orono Press, Orono, Me, USA, 1984. View at Google Scholar
  9. G. Barlow, The Cichlid Fishes: Nature's Grand Experiment In Evolution, Perseus Publishing, Cambridge, Mass, USA, 2000.
  10. P. Chakrabarty, “Testing conjectures about morphological diversity in cichlids of Lakes Malawi and Tanganyika,” Copeia, vol. 2, pp. 359–373, 2005. View at Google Scholar · View at Scopus
  11. R. Zardoya, D. M. Vollmer, C. Craddock, J. T. Streelman, S. A. Karl, and A. Meyer, “Evolutionary conservation of microsatellite flanking regions and their utility in resolving the phylogeny of cichlid fishes (Pisces: Perciformes),” Proceedings of the Royal Society London B, vol. 263, no. 1376, pp. 1589–1598, 1996. View at Google Scholar
  12. J. T. Streelman, R. Zardoya, A. Meyer, and S. A. Karl, “Multilocus phylogeny of cichlid fishes (Pisces: Perciformes): evolutionary comparison of microsatellite and single-copy nuclear loci,” Molecular Biology and Evolution, vol. 15, no. 7, pp. 798–808, 1998. View at Google Scholar · View at Scopus
  13. I. P. Farias, G. Orti, I. Sampaio, H. Schneider, and A. Meyer, “Mitochondrial DNA phylogeny of the family cichlidae: monophyly and fast molecular evolution of the neotropical assemblage,” Journal of Molecular Evolution, vol. 48, no. 6, pp. 703–711, 1999. View at Publisher · View at Google Scholar · View at Scopus
  14. I. P. Farias, G. Ortí, and A. Meyer, “Total evidence: molecules, morphology, and the phylogenetics of cichlid fishes,” Journal of Experimental Zoology, vol. 288, no. 1, pp. 76–92, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. J. S. Sparks, “Molecular phylogeny and biogeography of the Malagasy and South Asian cichlids (Teleostei: Perciformes: Cichlidae),” Molecular Phylogenetics and Evolution, vol. 30, no. 3, pp. 599–614, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Chakrabarty, “Cichlid biogeography: comment and review,” Fish and Fisheries, vol. 5, no. 2, pp. 97–119, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Katongo, S. Koblmüller, N. Duftner, L. Makasa, and C. Sturmbauer, “Phylogeography and speciation in the Pseudocrenilabrus philander species complex in Zambian rivers,” Hydrobiologia, vol. 542, no. 1, pp. 221–233, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. C. Katongo, S. Koblmüller, N. Duftner, L. Mumba, and C. Sturmbauer, “Evolutionary history and biogeographic affinities of the serranochromine cichlids in Zambian rivers,” Molecular Phylogenetics and Evolution, vol. 45, no. 1, pp. 326–338, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Koblmüller, K. M. Sefc, N. Duftner, C. Katongo, T. Tomljanovic, and C. Sturmbauer, “A single mitochondrial haplotype and nuclear genetic differentiation in sympatric colour morphs of a riverine cichlid fish,” Journal of Evolutionary Biology, vol. 21, no. 1, pp. 362–367, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. D. A. Joyce, D. H. Lunt, R. Bills et al., “An extant cichlid fish radiation emerged in an extinct Pleistocene lake,” Nature, vol. 435, no. 7038, pp. 90–95, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. O. Seehausen, “African cichlid fish: a model system in adaptive radiation research,” Proceedings of the Royal Society B, vol. 273, no. 1597, pp. 1987–1998, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Schluter, The Ecology of Adaptive Radiation, Oxford University Press, Oxford, UK, 2000.
  23. C. Sturmbauer, “Explosive speciation in cichlid fishes of the African Great Lakes: a dynamic model of adaptive radiation,” Journal of Fish Biology, vol. 53, supplement, pp. 18–36, 1998. View at Google Scholar · View at Scopus
  24. J. B. Yoder, E. Clancey, S. Des Roches et al., “Ecological opportunity and the origin of adaptive radiations,” Journal of Evolutionary Biology, vol. 23, no. 8, pp. 1581–1596, 2010. View at Google Scholar
  25. K. F. Liem, “Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws,” Systematic Biology, vol. 22, no. 4, pp. 425–441, 1973. View at Google Scholar
  26. N. B. Goodwin, S. Balshine-Earn, and J. D. Reynolds, “Evolutionary transitions in parental care in cichlid fish,” Proceedings of the Royal Society B, vol. 265, no. 1412, pp. 2265–2272, 1998. View at Google Scholar · View at Scopus
  27. M. L. J. Stiassny and A. Meyer, “Cichlids of the Rift lakes,” Scientific American, vol. 280, pp. 64–69, 1999. View at Google Scholar
  28. M. L. J. Stiassny, “Phylogenetic interrelationships of the family Cichlidae: an overview,” in Cichlid Fishes, Behaviour, Ecology and Evolution, M. H. A. Keenleyside, Ed., pp. 1–35, Chapman & Hall, London, UK, 1991. View at Google Scholar
  29. R. C. Albertson, J. A. Markert, P. D. Danley, and T. D. Kocher, “Phytogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 9, pp. 5107–5110, 1999. View at Google Scholar · View at Scopus
  30. C. Clabaut, P. M. Bunje, W. Salzburger, and A. Meyer, “Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations,” Evolution, vol. 61, no. 3, pp. 560–578, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. D. A. W. Thompson, On Growth and Form, Cambridge University Press, Cambridge, UK, 1917.
  32. F. L. Bookstein, Morphometric Tools for Landmark Data: Geometry and Biology, Cambridge University Press, New York, NY, USA, 1991.
  33. F. J. Rohlf and L. F. Marcus, “A revolution in morphometrics,” Trends in Ecology and Evolution, vol. 8, no. 4, pp. 129–132, 1993. View at Google Scholar · View at Scopus
  34. L. Rüber and D. C. Adams, “Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika,” Journal of Evolutionary Biology, vol. 14, no. 2, pp. 325–332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. F. J. Rohlf, “Morphometrics,” Annual Review of Ecology and Systematics, vol. 21, no. 1, pp. 299–316, 1990. View at Google Scholar · View at Scopus
  36. F. L. Bookstein, “Biometrics, biomathematics and the morphometric synthesis,” Bulletin of Mathematical Biology, vol. 58, no. 2, pp. 313–365, 1996. View at Google Scholar · View at Scopus
  37. D. C. Adams, F. J. Rohlf, and D. E. Slice, “Geometric morphometrics: ten years of progress following the “revolution”,” The Italian Journal of Zoology, vol. 71, no. 1, pp. 5–16, 2004. View at Google Scholar · View at Scopus
  38. M. L. Zelditch, D. L. Swidersky, H. D. Sheeds, and W. L. Fink, Geometric Morphometrics for Biologists: A Primer, Elsevier Academic Press, New York, NY, USA, 2004.
  39. D. E. Slice, “Geometric morphometrics,” Annual Review of Anthropology, vol. 36, no. 1, pp. 261–281, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Mitteroecker and P. Gunz, “Advances in geometric morphometrics,” Evolutionary Biology, vol. 36, no. 2, pp. 235–247, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. C. P. Klingenberg, “Evolution and development of shape: integrating quantitative approaches,” Nature Reviews Genetics, vol. 11, no. 9, pp. 623–635, 2010. View at Google Scholar
  42. A. M. Lawing and P. D. Polly, “Geometric morphometrics: recent applications to the study of evolution and development,” Journal of Zoology, vol. 280, no. 1, pp. 1–7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Bouton, F. Witte, and J. J. M. Van Alphen, “Experimental evidence for adaptive phenotypic plasticity in a rock-dwelling cichlid fish from Lake Victoria,” Biological Journal of the Linnean Society, vol. 77, no. 2, pp. 185–192, 2002. View at Publisher · View at Google Scholar · View at Scopus
  44. L. Postl, J. Herler, C. Bauer, M. Maderbacher, L. Makasa, and C. Sturmbauer, “Geometric morphometrics applied to viscerocranial bones in three populations of the Lake Tanganyika cichlid fish Tropheus moorii,” Journal of Zoological Systematics and Evolutionary Research, vol. 46, no. 3, pp. 240–248, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. C. J. Hellig, M. Kerschbaumer, K. M. Sefc, and S. Koblmüller, “Allometric shape change of the lower pharyngeal jaw correlates with a dietary shift to piscivory in a cichlid fish,” Naturwissenschaften, vol. 97, no. 7, pp. 663–672, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. F. L. Bookstein, “Applying landmark methods to biological outline data,” in Proceedings in Image Fusion and Shape Variability, K. V. Mardia, C. A. Gill, and I. L. Dryden , Eds., pp. 79–87, University of Leeds Press, Leeds, UK, 1996. View at Google Scholar
  47. P. Gunz, P. Mitteroecker, and F. L. Bookstein, “Semilandmarks in three dimensions,” in Modern Morphometrics in Physical Anthropology, D. E. Slice, Ed., pp. 73–98, Kluwer Academic/Plenum Publishers, New York, NY, USA, 2005. View at Google Scholar
  48. I. L. Dryden and K. V. Mardia, Statistical Shape Analysis, John Wiley & Sons, New York, NY, USA, 1998.
  49. D. D. Kassam, D. C. Adams, M. Hori, and K. Yamaoka, “Morphometric analysis on ecomorphologically equivalent cichlid species from Lakes Malawi and Tanganyika,” Journal of Zoology, vol. 260, no. 2, pp. 153–157, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Kassam, K. Yamaoka, B. Rusuwa, and M. Hori, “The robustness of geometric morphometrics in testing the morphological equivalence hypothesis among cichlid species from East African Great Lakes,” Biological Journal of the Linnean Society, vol. 91, no. 1, pp. 1–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. C. P. Klingenberg, M. Barluenga, and A. Meyer, “Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex,” Biological Journal of the Linnean Society, vol. 80, no. 3, pp. 397–408, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. K. J. Parsons, B. W. Robinson, and T. Hrbek, “Getting into shape,” Environmental Biology of Fishes, vol. 67, no. 4, pp. 417–431, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Trapani, “A morphometric analysis of polymorphism in the pharyngeal dentition of Cichlasoma minckleyi (Teleostei: Cichlidae),” Archives of Oral Biology, vol. 49, no. 10, pp. 825–835, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Maderbacher, C. Bauer, J. Herler, L. Postl, L. Makasa, and C. Sturmbauer, “Assessment of traditional versus geometric morphometrics for discriminating populations of the Tropheus moorii species complex (Teleostei: Cichlidae), a Lake Tanganyika model for allopatric speciation,” Journal of Zoological Systematics and Evolutionary Research, vol. 46, no. 2, pp. 153–161, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. R. C. Albertson and T. D. Kocher, “Assessing morphological differences in an adaptive trait: a landmark-based morphometric approach,” Journal of Experimental Zoology, vol. 289, no. 6, pp. 385–403, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. R. C. Albertson, J. T. Streelman, and T. D. Kocher, “Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5252–5257, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. R. C. Albertson, J. T. Streelman, and T. D. Kocher, “Genetic basis of adaptive shape differences in the cichlid head,” Journal of Heredity, vol. 94, no. 4, pp. 291–301, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. R. C. Albertson, J. T. Streelman, T. D. Kocher, and P. C. Yelick, “Integration and evolution of the cichlid mandible: the molecular basis of alternate feeding strategies,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 45, pp. 16287–16292, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. D. D. Kassam, D. C. Adams, and K. Yamaoka, “Functional significance of variation in trophic morphology within feeding microhabitat-differentiated cichlid species in Lake Malawi,” Animal Biology, vol. 54, no. 1, pp. 77–90, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. J. T. Streelman, R. C. Albertson, and T. D. Kocher, “Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi,” Freshwater Biology, vol. 52, no. 3, pp. 525–538, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Barluenga, K. N. Stölting, W. Salzburger, M. Muschick, and A. Meyer, “Sympatric speciation in Nicaraguan crater lake cichlid fish,” Nature, vol. 439, no. 7077, pp. 719–723, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. C. D. Hulsey, R. J. Roberts, A. S. P. Lin, R. Guldberg, and J. T. Streelman, “Convergence in a mechanically complex phenotype: detecting structural adaptations for crushing in cichlid fish,” Evolution, vol. 62, no. 7, pp. 1587–1599, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. C. P. Klingenberg, M. Barluenga, and A. Meyer, “Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry,” Evolution, vol. 56, no. 10, pp. 1909–1920, 2002. View at Google Scholar · View at Scopus
  64. E. Marquez, “Sage: symmetry and asymmetry in geometric data,” http://www-personal.umich.edu/~emarquez/morph/.
  65. C. P. Klingenberg, “MorphoJ: an integrated software package for geometric morphometrics,” http://www.flywings.org.uk/MorphoJ_page.htm.
  66. T. J. M. Van Dooren, H. A. Van Goor, and M. Van Putten, “Handedness and asymmetry in scale-eating cichlids: antisymmetries of different strength,” Evolution, vol. 64, no. 7, pp. 2159–2165, 2010. View at Google Scholar
  67. J. S. Huxley, “Constant differential growth-ratios and their significance,” Nature, vol. 114, no. 2877, pp. 895–896, 1924. View at Google Scholar · View at Scopus
  68. S. J. Gould, “Allometry and size in ontogeny and phylogeny,” Biological Reviews, vol. 41, no. 4, pp. 587–640, 1966. View at Google Scholar · View at Scopus
  69. S. J. Gould, Ontogeny and Phylogeny, Harvard University Press, Cambridge, Mass, USA, 1977.
  70. K. Fujimura and N. Okada, “Shaping of the lower jaw bone during growth of Nile tilapia Oreochromis niloticus and a Lake Victoria cichlid Haplochromis chilotes: a geometric morphometric approach,” Development Growth & Differentiation, vol. 50, no. 8, pp. 653–663, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. R. F. Oliveira and V. C. Almada, “Sexual dimorphism and allometry of external morphology in Oreochromis mossambicus,” Journal of Fish Biology, vol. 46, no. 6, pp. 1055–1064, 1995. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Erlandsson and A. J. Ribbink, “Patterns of sexual size dimorphism in African cichlid fishes,” South African Journal of Science, vol. 93, no. 11-12, pp. 498–508, 1997. View at Google Scholar · View at Scopus
  73. D. Schütz and M. Taborsky, “Giant males or dwarf females: what determines the extreme sexual size dimorphism in Lamprologus callipterus?” Journal of Fish Biology, vol. 57, no. 5, pp. 1254–1265, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Ota, M. Kohda, and T. Sato, “Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females,” Journal of Biosciences, vol. 35, no. 2, pp. 257–265, 2010. View at Google Scholar
  75. D. Kassam, S. Mizoiri, and K. Yamaoka, “Interspecific variation of body shape and sexual dimorphism in three coexisting species of the genus petrotilapia (Teleostei: Cichlidae) from Lake Malawi,” Ichthyological Research, vol. 51, no. 3, pp. 195–201, 2004. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Herler, M. Kerschbaumer, P. Mitteroecker, L. Postl, and C. Sturmbauer, “Sexual dimorphism and population divergence in the Lake Tanganyika cichlid fish genus Tropheus,” Frontiers in Zoology, vol. 7, article 4, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. T. A. Stewart and R. C. Albertson, “Evolution of a unique predatory feeding apparatus: functional anatomy, development and a genetic locus for jaw laterality in Lake Tanganyika scale-eating cichlids,” BMC Biology, vol. 8, article 8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. R. Takahashi, K. Watanabe, M. Nishida, and M. Hori, “Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach,” BMC Evolutionary Biology, vol. 7, no. 1, article 195, 2007. View at Publisher · View at Google Scholar · View at Scopus
  79. W. J. Cooper, K. Parsons, A. McIntyre, B. Kern, A. McGee-Moore, and R. C. Albertson, “Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African Rift-Lakes,” PLoS ONE, vol. 5, article e9551, no. 3, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. K. A. Young, J. Snoeks, and O. Seehausen, “Morphological diversity and the roles of contingency, chance and determinism in African cichlid radiations,” PLoS ONE, vol. 4, article e4740, no. 3, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. K. J. Parsons, W. J. Cooper, and R. C. Albertson, “Limits of principal components analysis for producing a common trait space: Implications for inferring selection, contingency, and chance in evolution,” PLoS ONE, vol. 4, article e7957, no. 11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. R. B. Stelkens, C. Schmid, O. Selz, and O. Seehausen, “Phenotypic novelty in experimental hybrids is predicted by the genetic distance between species of cichlid fish,” BMC Evolutionary Biology, vol. 9, article 283, 2009. View at Publisher · View at Google Scholar