Constraint and opportunity: The genetic basis and evolution of modularity in the cichlid mandible

American Naturalist

Volumn 179, Issue 1, 2012, Pages 64-78

  Parsons, Kevin J ^a,b   Márquez, Eladio ^c   Craig Albertson, R ^a,b  

^a SYRACUSE UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Development; Evolvability; Functional morphology; Phenotypic integration

Indexed keywords

BONE; CICHLID; CLADISTICS; ECOTYPE; EVOLUTIONARY BIOLOGY; FEEDING MECHANISM; FUNCTIONAL MORPHOLOGY; GENETIC STRUCTURE; HERITABILITY; PHENOTYPE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMETRY; CICHLID; COMPUTER SIMULATION; EVALUATION; EVOLUTION; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HYBRIDIZATION; LAKE; MALAWI; MANDIBLE; METHODOLOGY; MOZAMBIQUE; PHYSIOLOGY; QUANTITATIVE TRAIT LOCUS; SPECIES DIFFERENCE;

ANIMALS; BIOLOGICAL EVOLUTION; BIOMETRY; CICHLIDS; COMPUTER SIMULATION; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYBRIDIZATION, GENETIC; LAKES; MALAWI; MANDIBLE; MODELS, BIOLOGICAL; MOZAMBIQUE; QUANTITATIVE TRAIT LOCI; SPECIES SPECIFICITY;

EAST AFRICAN LAKES; LAKE MALAWI;

EID: 83655172673     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/663200     Document Type: Article

References (81)

1. Abzhanov, A., M. Protas, B. R. Grant, P. R. Grant, and C. J. Tabin. 2004. Bmp4 and morphological variation of beaks in Darwin's finches. Science 305:1462-1465.
2. Albertson, R. C., J. T. Streelman, and T. D. Kocher. 2003. Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proceedings of the National Academy of Sciences of the USA 100: 5252-5257.
3. Albertson, R. C., J. T. Streelman, T. D. Kocher, and P. C. Yelick. 2005. Integration and evolution of the cichlid mandible: molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences of the USA 102:16287-16292.
4. Arnegard, M. E., P. B. McIntyre, L. J. Harmon, M. L. Zelditch, W. G. R. Crampton, J. K. Davis, J. P. Sullivan, S. Lavoué, and C. D. Hopkins. 2010. Sexual signal evolution outpaces ecological divergence during electric fish species radiation. American Naturalist 176:335-356.
5. Atchley, W. R., and B. K. Hall. 1991. A model for the development and evolution of complex morphological structures. Biological Reviews 166:101-157.
6. Barel, C. D. N., F. Witte, and M. J. P. Van Oijen. 1976. The shape of the skeletal elements in the head of a generalized Haplochromis species: H. elegans trewas 1933 (Pisces, Cichlidae). Netherlands Journal of Zoology 26:163-265.
7. Berner, D., C. Adams, A. C. Grandchamp, and A. P. Hendry. 2008. Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology. Journal of Evolutionary Biology 21: 1653-1665.
8. Bookstein, F. L. 1997. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis 1:225-243.
9. Chenoweth, S. F., H. D. Rundle, and M. W. Blows. 2010. The contribution of selection and genetic constraints to phenotypic divergence. American Naturalist 175:186-196.
10. Cheverud, J. M. 1982. Relationships among ontogenic, static, and evolutionary allometry. American Journal of Physical Anthropology 59:139-149.
11. Cheverud, J. M. 1984. Quantitative genetics and developmental constraints on evolution by selection. Journal of Theoretical Biology 110:155-171.
12. Cheverud, J. M. 1996. Developmental integration and the evolution of pleiotropy. American Zoologist 36:44-50.
13. Cheverud, J. M. 1997. Pleiotropic effects of individual gene loci on mandibular morphology. Evolution 51:2004-2014.
14. Claverie, T., E. Chan, and S. N. Patek. 2011. Modularity and scaling in fast movements: power amplification in mantis shrimp. Evolution 65:443-461.
15. Collar, D. C., and P. C. Wainwright. 2009. Ecomorphology of the Centrarchidae. Pages 70-89 in S. J. Cook and D. P. Philipp, eds. Centrarchid fishes: diversity, biology and conservation. Blackwell Scientific, Cambridge.
16. Conner, J. K. 2002. Genetic mechanisms of floral trait correlations in a natural population. Nature 420:407-410.
17. Cooper, W. J., and M. W. Westneat. 2009. Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evolutionary Biology 9:24.
18. Cooper, W. J., K. Parsons, A. McIntyre, B. Kern, A. McGee-Moore, and R. C. Albertson. 2010. Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLoS ONE 5:e9551.
19. Crawley, M. J. 2007. The R book. Wiley, New York.
20. Ehlinger, T. J., and D. S. Wilson. 1988. A complex foraging polymorphism in bluegill sunfish. Proceedings of the National Academy of Sciences of the USA 85:1878-1882.
21. Enlow, D. H., and M. G. Hans. 1996. Essentials of facial growth. Saunders, Philadelphia.
22. Fraser, G. J., C. D. Hulsey, R. F. Bloomquist, K. Uyesugi, N. R. Manley, and J. T. Streelman. 2009. An ancient gene network is co-opted for teeth on old and new jaws. PloS Biology 7:e1000031.
23. Fujimura, K., and F. Okada. 2007. Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae): developmental staging system. Development, Growth and Differentiation 49:301-324.
24. Hall, B. K., and T. Miyake. 2000. All for one and one for all: condensations and the initiation of skeletal development. BioEssays 22:138-147.
25. Herring, S. W. 1993. Epigenetic and functional influences on skull growth. Pages 153-206 in J. Hanken and B. K. Hall, eds. The skull. University of Chicago Press, Chicago.
26. Klingenberg, C. P. 2008. Morphological integration and developmental modularity. Annual Reviews of Ecology Evolution and Systematics 39:115-132.
27. Klingenberg, C. P. 2010. Evolution and development of shape: integrating quantitative approaches. Nature Reviews Genetics 11:623-635.
28. Klingenberg, C. P., A. V. Badyaev, S. M. Sowry, and N. J. Beckwith. 2001. Inferring developmental modularity from morphological integration: analysis of individual variation and asymmetry in bumblebee wings. American Naturalist 157:11-23.
29. Klingenberg, C. P., K. Mebus, and J. C. Auffray. 2003. Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evolution and Development 5:522-531.
30. Klingenberg, C. P., L. J. Leamy, and J. M. Cheverud. 2004. Integration and modularity of quantitative trait locus effects on geometric shape in the mouse mandible. Genetics 166:1909-1921.
31. Kocher, T. D. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5:288-298.
32. Konings, A. 2001. Malawi cichlids in their natural habitat. Cichlid, El Paso, TX.
33. Krzanowski, W. J. 2000. Principles of multivariate analysis: a user's perspective. Oxford University Press, Oxford.
34. Lee, B. Y., W. J. Lee, J. T. Streelman, K. L. Carleton, A. E. Howe, G. Hulata, A. Slettan, J. E. Stern, Y. Terai, and T. D. Kocher. 2005. A second generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237-244.
35. Leroi, A. M. 2000. The scale independence of evolution. Evolution and Development 2:67-77.
36. Liem, K. F. 1991. Functional morphology. Pages 129-145 in M. H. A. Keenleyside, ed. Cichlid fishes: behaviour, ecology and evolution. Chapman & Hall, New York.
37. Loh, Y.-H. E., L. S. Katz, M. C. Mims, T. D. Kocher, S. V. Yi, and J. T. Streelman. 2008. Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology 9:R113.
38. Manly, B. F. J. 2006. Randomization, bootstrap and Monte Carlo methods in biology. 3rd ed. Chapman & Hall/CRC, Boca Raton, FL.
39. Márquez, E. J. 2008. A statistical framework for testing modularity in multidimensional data. Evolution 62:2688-2708.
40. Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert. 1985. Developmental constraints and evolution: a perspective from the Mountain Lake conference on development and evolution. Quarterly Review of Biology 60:265-287.
41. Mayr, E. 1954. Change of genetic environment and evolution. Pages 157-180 in J. Huxley, A. C. Hardy and E. B. Ford, eds. Evolution as a process. Allen & Unwin, London.
42. Mezey, J., J. Cheverud, and G. Wagner. 2000. Is the genotype-phenotype map modular? an approach using quantitative trait locus (QTL) data. Genetics 156:305-311.
43. Miller, R. G. 1974. The jackknife: a review. Biometrika 61:1-15.
44. Monteiro, L. R., and M. R. Nogueira. 2010. Adaptive radiations, ecological specialization, and the evolutionary integration of complex morphological structures. Evolution 64:724-744.
45. Olson, E. C., and R. L. Miller. 1958. Morphological integration. University of Chicago Press, Chicago.
46. Parsons, K. J., and B. W. Robinson. 2006. Replicated evolution of divergent integrated plastic responses during early adaptive divergence. Evolution 60:801-813.
47. Parsons, K. J., and B. W. Robinson. 2007. Foraging performance of diet-induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism. Journal of Evolutionary Biology 20:673-684.
48. Pavlicev, M., J. M. Cheverud, and G. P. Wagner. 2009. Measuring morphological integration using eigenvalue variance. Evolutionary Biology 36:157-170.
49. Pigliucci, M. 2008. Is evolvability evolvable? Nature Reviews Genetics 9:75-82.
50. Pigliucci, M., and K. Preston. 2004. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, Oxford.
51. Potvin, C., and D. A. Roff. 1993. Distribution-free and robust statistical methods: viable alternatives to parametric statistics? Ecology 74:1617-1628.
52. Ribbink, A. J., B. A. Marsh, A. C. Marsh, A. C. Ribbink, and B. J. Sharp. 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology 18: 149-310.
53. Richtsmeier, J. T., T. M. Cole III, and S. Lele. 2005. Landmark morphometrics and the analysis of variation. Pages 49-68 in B. Hallgrimsson and B. K. Hall, eds. Variation: a central concept in biology. Elsevier Academic, Boston.
54. Robinson, B. W., D. S. Wilson, A. S. Margosian, and P. T. Lotito. 1993. Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evolutionary Ecology 7:451-464.
55. Robinson, B. W., D. S. Wilson, and G. O. Shea. 1996. Trade-offs of ecological specialization: an intraspecific comparison of pumpkinseed sunfish phenotypes. Ecology 77:170-178.
56. Roff, D. 2002. Comparing G matrices: a MANOVA approach. Evolution 56:1286-1291.
57. Rohlf, F. J. 2009. tpsDIG2, a software program for landmark data acquisition. http://life.bio.sunysb.edu/morph/.
58. Rohlf, F. J., and D. Slice. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology 39:40-59.
59. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774.
60. Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, Oxford.
61. Sheets, H. D. 2002. Standard6: a program for minimizing allometric effects in landmark data. http://www3.canisius.edu/sheets/morphsoft.html.
62. Sheets, H. D. 2009. Semiland6: a tool for processing semi-landmarks, prior to use in other programs. http://www3.canisius.edu/sheets/morphsoft.html.
63. Streelman, J. T., and R. C. Albertson. 2006. Evolution of novelty in the cichlid dentition. Journal of Experimental Zoology 306:216-226.
64. Van Ooijen, J. W. 2004. MapQTL 5, software for the mapping of quantitative trait loci in experimental populations. Kyazma, Wageningen.
65. Van Valen, L. 1965. The study of morphological integration. Evolution 19:347-349.
66. Wagner, G. P. 1996. Homologues, natural kinds and the evolution of modularity. American Zoologist 36:36-43.
67. Wagner, G. P., and L. Altenberg. 1996. Complex adaptations and the evolution of evolvability. Evolution 50:967-976.
68. Wagner, G. P., M. Pavlicev, and J. M. Cheverud. 2007. The road to modularity. Nature Reviews Genetics 8:921-931.
69. Webster, M., and M. L. Zelditch. 2011. Modularity of a Cambrian ptychoparioid trilobite cranidium. Evolution and Development 13: 96-109.
70. West-Eberhard, M. J. 2003. Developmental plasticity and evolution. Oxford University Press, Oxford.
71. Westneat, M. W. 1991. Linkage biomechanics and evolution of the jaw protrusion mechanism of the sling-jaw wrasse, Epibulus insidiator. Journal of Experimental Biology 159:165-184.
72. Westneat, M. W. 2003. A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. Journal of Theoretical Biology 223:269-281.
73. Westneat, M. W., M. E. Alfaro, P. C. Wainwright, D. R. Bellwood, J. R. Grubich, J. L. Fessler, K. D. Clements, and L. L. Smith. 2005. Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae. Proceedings of the Royal Society B: Biological Sciences 272: 993-1000.
74. Wu, P., T. X. Jiang, S. Suksaweang, R. B. Widelitz, and C. M. Chuong. 2004. Molecular shaping of the beak. Science 305:1465-1466.
75. Wu, P., T. X. Jiang, J. Y. Shen, R. B. Widelitz, and C. M. Chuong. 2006. Morphoregulation of avian beaks: comparative mapping of growth zone activities and morphological evolution. Developmental Dynamics 235:1400-1412.
76. Young, K. A., J. Snoeks, and O. Seehausen. 2009. Morphological diversity and the roles of contingency, chance and determinism in African cichlid radiations. PLoS ONE 4:e4740.
77. Young, R. L., and A. V. Badyaev. 2007. Evolution of ontogeny: linking epigenetic remodelling and genetic adaptation in skeletal structures. Integrative and Comparative Biology 47:234-244.
78. Zelditch, M. L., D. L. Swiderski, H. D. Sheets, and W. L. Fink. 2004. Geometric morphometrics for biologists: a primer. Elsevier Academic, London.
79. Zelditch, M. L., A. R. Wood, R. M. Bonett, and D. L. Swiderski. 2008. Modularity of the rodent mandible: integrating bones, muscles, and teeth. Evolution and Development 10:756-768.
80. Zelditch, M. L., A. R. Wood, and D. L. Swiderski. 2009. Building developmental integration into functional systems: functioninduced integration of mandibular shape. Evolutionary Biology 36:71-87.
81. Zimmerman, M. S., S. N. Schmidt, C. C. Krueger, M. J. Vander Zanden, and R. L. Eshenroder. 2009. Ontogenetic niche shifts and resource partitioning of lake trout morphotypes. Canadian Journal of Fisheries and Aquatic Sciences 66:1007-1018.