Table of Contents
International Journal of Evolutionary Biology
Volume 2012, Article ID 538146, 9 pages
http://dx.doi.org/10.1155/2012/538146
Research Article

More than Meets the Eye: Functionally Salient Changes in Internal Bone Architecture Accompany Divergence in Cichlid Feeding Mode

1Department of Biology, University of Massachusetts Amherst, 611 North Pleasant Street, Amherst, MA 01003, USA
2School of Biological Sciences, Washington State University Tri-Cities, 2710 Crimson Way, Richland, WA 99354, USA
3Institute for Human Performance, Department of Orthopedic Surgery, SUNY Upstate Medical University, 750 East Adams Street, Syracuse, NY 13210, USA

Received 17 January 2012; Accepted 14 March 2012

Academic Editor: Tetsumi Takahashi

Copyright © 2012 R. Craig Albertson et al. 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. D. Schluter, The Ecology of Adaptive Radiations, Oxford University Press, Oxford, UK, 2000.
  2. B. G. Baldwin and M. J. Sanderson, “Age and rate of diversification of the Hawaiian silversword alliance (Compositae),” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 16, pp. 9402–9406, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. G. D. Carr, Monograph of the Hawaiian Madiinae (Asteraceae): Argyroxiphium, Dubautia, and Wilkesia. Allertonia, vol. 4, Pacific Tropical Botanical Garden, 1985.
  4. R. Calsbeek and D. J. Irschick, “The quick and the dead: Correlational selection on morphology, performance, and habitat use in island lizards,” Evolution, vol. 61, no. 11, pp. 2493–2503, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Huyghe, A. Herrel, B. Vanhooydonck, J. J. Meyers, and D. J. Irschick, “Microhabitat use, diet, and performance data on the Hispaniolan twig anole, Anolis sheplani: pushing the boundaries of morphospace,” Zoology, vol. 110, no. 1, pp. 2–8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. B. Langerhans, J. H. Knouft, and J. B. Losos, “Shared and unique features of diversification in greater Antillean Anolis ecomorphs,” Evolution, vol. 60, no. 2, pp. 362–369, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. B. Losos, T. W. Schoener, K. I. Warheit, and D. Creer, “Experimental studies of adaptive differentiation in Bahamian Anolis lizards,” Genetica, vol. 112-113, pp. 399–415, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. J. B. Losos, “Integrative approaches to evolutionary ecology: anolis lizards as model systems,” Annual Review of Ecology and Systematics, vol. 25, pp. 467–493, 1994. View at Google Scholar · View at Scopus
  9. P. R. Grant and B. R. Grant, “Evolution of character displacement in Darwin's finches,” Science, vol. 313, no. 5784, pp. 224–226, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Sato, C. O'huigin, F. Figueroa et al., “Phylogeny of Darwin's finches as revealed by mtDNA sequences,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 9, pp. 5101–5106, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Sato, H. Tichy, C. O'Huigin, P. R. Grant B, R. Grant, and J. Klein, “On the origin of Darwin's finches,” Molecular Biology and Evolution, vol. 18, no. 3, pp. 299–311, 2001. View at Google Scholar · View at Scopus
  12. R. C. Albertson and T. D. Kocher, “Genetic and developmental basis of cichlid trophic diversity,” Heredity, vol. 97, no. 3, pp. 211–221, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. 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
  14. 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, no. 3, Article ID e9551, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Kornfield and P. F. Smith, “African cichlid fishes: model systems for evolutionary biology,” Annual Review of Ecology and Systematics, vol. 31, pp. 163–196, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. T. D. Kocher, “Adaptive evolution and explosive speciation: the cichlid fish model,” Nature Reviews Genetics, vol. 5, no. 4, pp. 288–298, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. K. F. Liem, “Functional morphology,” in Cichlid Fishes: Behavior, Ecology and Evolution, M. H. A. Keenleyside, Ed., pp. 129–150, Chapman and Hall, London, UK, 1991. View at Google Scholar
  18. A. Herrel, J. Podos, B. Vanhooydonck, and A. P. Hendry, “Force-velocity trade-off in Darwin's finch jaw function: a biomechanical basis for ecological speciation?” Functional Ecology, vol. 23, no. 1, pp. 119–125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. J. Podos and S. Nowicki, “Beaks, adaptation, and vocal evolution in Darwin's finches,” BioScience, vol. 54, no. 6, pp. 501–510, 2004. View at Google Scholar · View at Scopus
  20. P. Chakrabarty, “Testing conjectures about morphological diversity in cichlids of Lakes Malawi and Tanganyika,” Copeia, no. 2, pp. 359–373, 2005. View at Google Scholar · View at Scopus
  21. 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, no. 3, Article ID e4740, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. W. J. Cooper and M. W. Westneat, “Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches,” BMC Evolutionary Biology, vol. 9, no. 1, article 24, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. P. C. Wainwright and B. A. Richard, “Predicting patterns of prey use from morphology of fishes,” Environmental Biology of Fishes, vol. 44, no. 1–3, pp. 97–113, 1995. View at Publisher · View at Google Scholar · View at Scopus
  24. M. W. Westneat, “A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes,” Journal of Theoretical Biology, vol. 223, no. 3, pp. 269–281, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. M. W. Westneat, M. E. Alfaro, P. C. Wainwright et al., “Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae,” Proceedings of the Royal Society B, vol. 272, no. 1567, pp. 993–1000, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. D. C. Collar, B. C. O'Meara, P. C. Wainwright, and T. J. Near, “Piscivory limits diversification of feeding morphology in centrarchid fishes,” Evolution, vol. 63, no. 6, pp. 1557–1573, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. A. N. Rice, W. J. Cooper, and M. W. Westneat, “Diversification of coordination patterns during feeding behaviour in cheiline wrasses,” Biological Journal of the Linnean Society, vol. 93, no. 2, pp. 289–308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. M. W. Westneat, “Transmission of force and velocity in the feeding mechanisms of labrid fishes (Teleostei, Perciformes),” Zoomorphology, vol. 114, no. 2, pp. 103–118, 1994. View at Publisher · View at Google Scholar · View at Scopus
  29. C. D. Hulsey and F. J. García De León, “Cichlid jaw mechanics: linking morphology to feeding specialization,” Functional Ecology, vol. 19, no. 3, pp. 487–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. T. B. Waltzek and P. C. Wainwright, “Functional morphology of extreme jaw protrusion in neotropical cichlids,” Journal of Morphology, vol. 257, no. 1, pp. 96–106, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. L. A. Ferry-Graham, P. C. Wainwright, and D. R. Bellwood, “Prey capture in long-jawed butterflyfishes (Chaetodontidae): the functional basis of novel feeding habits,” Journal of Experimental Marine Biology and Ecology, vol. 256, no. 2, pp. 167–184, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. M. W. Westneat, “Feeding mechanics of teleost fishes (Labridae; Perciformes): a test of four-bar linkage models,” Journal of Morphology, vol. 205, no. 3, pp. 269–295, 1990. View at Publisher · View at Google Scholar · View at Scopus
  33. M. W. Westneat, “Skull biomechanics and suction feeding in fishes,” in Fish Biomechanics, R. E. Shadwick and G. V. Lauder, Eds., Elsevier Academic Press, San Diego, Calif, USA, 2006. View at Google Scholar
  34. W. J. Cooper, J. Wernle, K. Mann, and R. C. Albertson, “Functional and Genetic Integration in the Skulls of Lake Malawi Cichlids,” Evolutionary Biology, vol. 38, no. 3, pp. 316–334, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. E. R. Dumont, “Feeding mechanisms in bats: variation within the constraints of flight,” Integrative and Comparative Biology, vol. 47, no. 1, pp. 137–146, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. D. S. Strait, G. W. Weber, S. Neubauer et al., “The feeding biomechanics and dietary ecology of Australopithecus africanus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 7, pp. 2124–2129, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Herrel, S. E. Vincent, M. E. Alfaro, S. Van Wassenbergh, B. Vanhooydonck, and D. J. Irschick, “Morphological convergence as a consequence of extreme functional demands: examples from the feeding system of natricine snakes,” Journal of Evolutionary Biology, vol. 21, no. 5, pp. 1438–1448, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Herrel, B. Vanhooydonck, K. Huyghe, R. Van Damme, and D. J. Irschick, “Rapid evolutionary divergence in feeding mechanics after the colonization of new environments in lizards,” Comparative Biochemistry and Physiology, vol. 148, p. S52, 2007. View at Google Scholar
  39. A. Herrel, P. Aerts, J. Fret, and F. de Vree, “Morphology of the feeding system in agamid lizards: ecological correlates,” Anatomical Record, vol. 254, no. 4, pp. 496–507, 1999. View at Google Scholar
  40. 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
  41. A. P. Summers, R. A. Ketcham, and T. Rowe, “Structure and function of the horn shark (Heterodontus francisci) cranium through ontogeny: development of a hard prey specialist,” Journal of Morphology, vol. 260, no. 1, pp. 1–12, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. 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
  43. A. J. Ribbink, B. A. Marsh, A. C. Marsh, A. C. Ribbink, and B. J. Sharp, “A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi,” South African Journal of Zoology, vol. 18, no. 3, pp. 149–310, 1983. View at Google Scholar · View at Scopus
  44. Catalog of Fishes electronic version, http://research.calacademy.org/ichthyology/catalog/fishcatsearch.html.
  45. E. Otten, “The jaw mechanism during growth of a generalized Haplochromis species: H. Elegans trewavas 1933 (Pisces, Cichlidae),” Netherlands Journal of Zoology, vol. 33, pp. 55–98, 1983. View at Google Scholar
  46. C. D. N. Barel, F. Witte, and M. J. W. Van Ooijen, “The shape of the skeletal elements in the head of a generalized Haplochromis species: H. elegans Trewavas 1933 (Pisces, Cichlidae),” Netherlands Journal of Zoology, vol. 26, no. 2, pp. 163–265, 1976. View at Google Scholar
  47. 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
  48. 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
  49. J. W. Van Ooijen and R. E. Voorrips, “JoinMap 3.0: software for the calculation of genetic linkage maps,” in Plant Research International, Wageningen UR, Wageningen, The Netherlands, 2001. View at Google Scholar
  50. J. W. Van Ooijen, M. P. Boer, R. C. Jansen, and C. Maliepaard, “QTLMap 4.0: Software for the calculation of QTL positions on genetic maps,” in Plant Research International, Wageningen UR, Wageningen, The Netherlands, 2002. View at Google Scholar
  51. W. D. Beavis, “The power and deceit of QTL experiments: lessons from comparative QTL studies,” in Proceedings of the 49th Annual Corn and Sorghum Research Conference, pp. 252–268, American Seed Trade Association, Washington, DC, USA, 1994.
  52. W. D. Beavis, “QTL analyses: power, precision, and accuracy,” in Molecular Dissection of Complex Traits, A. H. Paterson, Ed., pp. 145–161, CRC Press, Boca Raton, Fla, USA, 1998. View at Google Scholar
  53. A. H. Price, “Believe it or not, QTLs are accurate!,” Trends in Plant Science, vol. 11, no. 5, pp. 213–216, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. 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
  55. K. Parsons, E. Marquez, and R. C. Albertson, “Constraint and opportunity: the genetic basis and evolution of modularity in the cichlid mandible,” American Naturalist, vol. 179, no. 1, pp. 64–78, 2012. View at Google Scholar
  56. R. A. Anderson, L. D. Mcbrayer, and A. Herrel, “Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure,” Biological Journal of the Linnean Society, vol. 93, no. 4, pp. 709–720, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. A. A. Biewener, “Biomechanical consequences of scaling,” Journal of Experimental Biology, vol. 208, no. 9, pp. 1665–1676, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. J. D. Currey, Bones: Structure and Mechanics, Princeton University Press, Princeton, NJ, USA, 2002.
  59. R. Huiskes, R. Rulmerman, G. H. Van Lenthe, and J. D. Janssen, “Effects of mechanical forces on maintenance and adaptation of form in trabecular bone,” Nature, vol. 405, no. 6787, pp. 704–706, 2000. View at Publisher · View at Google Scholar · View at Scopus
  60. J. D. Currey and R. M. Alexander, “The thickness of the walls of tubular bones,” Journal of Zoology, vol. 206, pp. 453–468, 1985. View at Google Scholar
  61. E. R. Dumont, “Bone density and the lightweight skeletons of birds,” Proceedings of the Royal Society B, vol. 277, no. 1691, pp. 2193–2198, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. S. M. Swartz, M. B. Bennett, and D. R. Carrier, “Wing bone stresses in free flying bats and the evolution of skeletal design for flight,” Nature, vol. 359, no. 6397, pp. 726–729, 1992. View at Publisher · View at Google Scholar · View at Scopus
  63. N. M. Gray, K. Kainec, S. Madar, L. Tomko, and S. Wolfe, “Sink or swim? Bone density as a mechanism for buoyancy control in early cetaceans,” Anatomical Record, vol. 290, no. 6, pp. 638–653, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Ricqles and V. Buffrenil, “Bone histology, heterochronies and the return of Tetrapods to life in water: where are we?” in Secondary Adaptation of Tetrapods to Life in Water, J.-M. Mazin and V. Buffrenil, Eds., pp. 289–306, Verlag Dr. Friedrich Pfeil, Munchen, Germany, 2001. View at Google Scholar
  65. O. S. Voskoboynikova, “Evolution of the visceral skeleton and phylogeny of Nototheniidae,” Journal of Ichthyology, vol. 33, pp. 23–47, 1993. View at Google Scholar
  66. J. T. Eastman and A. R. McCune, “Fishes on the Antarctic continental shelf: Evolution of a marine species flock?” Journal of Fish Biology, vol. 57, pp. 84–102, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. J. T. Eastman, “The nature of the diversity of Antarctic fishes,” Polar Biology, vol. 28, no. 2, pp. 93–107, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. J. T. Eastman, Antarctic Fish Biology: Evolution in a Unique Environment, Academic Press, San Diego, Calif, USA, 1993.
  69. J. T. Eastman, “Phyletic devergence and specialization for pelagiclife in the Antarctic nototheniid fish Pleuragrammaan tarcticum,” Comparative Biochemistry and Physiology, vol. 118, no. 4, pp. 1095–1101, 1997. View at Publisher · View at Google Scholar · View at Scopus
  70. R. C. Albertson, Y. L. Yan, T. A. Titus et al., “Molecular pedomorphism underlies craniofacial skeletal evolution in Antarctic notothenioid fishes,” BMC Evolutionary Biology, vol. 10, no. 1, article 4, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. O. S. Voskoboynikova, “Rates of individual development of the bony skeleton of eleven species of the family Nototheniidae,” Journal of Ichthyology, vol. 34, pp. 108–120, 1994. View at Google Scholar
  72. O. S. Voskoboynikova, O. Y. Tereshchuk, and A. Kellermann, “Osteological development of the Antarctic silverfish Pleuragramma antarcticum (Nototheniidae),” Cybium, vol. 18, pp. 251–271, 1994. View at Google Scholar
  73. J. N. Dowthwaite, R. M. Hickman, J. A. Kanaley, R. J. Ploutz-Snyder, J. A. Spadaro, and T. A. Scerpella, “Distal radius strength: a comparison of DXA-derived vs pQCT-measured parameters in adolescent females,” Journal of Clinical Densitometry, vol. 12, no. 1, pp. 42–53, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. J. N. Dowthwaite and T. A. Scerpella, “Skeletal geometry and indices of bone strength in artistic gymnasts,” Journal of Musculoskeletal Neuronal Interactions, vol. 9, no. 4, pp. 198–214, 2009. View at Google Scholar · View at Scopus
  75. P. Chavassieux, E. Seeman, and P. D. Delmas, “Insights into material and structural basis of bone fragility from diseases associated with fractures: how determinants of the biomechanical properties of bone are compromised by disease,” Endocrine Reviews, vol. 28, no. 2, pp. 151–164, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. M. C. H. Van der Meulen, K. J. Jepsen, and B. Miki, “Understanding bone strength: size isn't everything,” Bone, vol. 29, no. 2, pp. 101–104, 2001. View at Publisher · View at Google Scholar · View at Scopus