The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (family: Balistidae)

Evolution

Volumn 65, Issue 7, 2011, Pages 1912-1926

  Dornburg, Alex ^a   Sidlauskas, Brian ^b,c   Santini, Francesco ^d   Sorenson, Laurie ^e   Near, Thomas J ^a   Alfaro, Michael E ^d  

^a YALE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c NATIONAL EVOLUTIONARY SYNTHESIS CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e VIRGINIA INSTITUTE OF MARINE SCIENCE   (United States)

Author keywords

Adaptive radiation; Balistiform; Correlated evolution; Disparity; Generalized least squares; Geometric morphometrics; Locomotion; Tetraodontiformes

Indexed keywords

ADAPTIVE RADIATION; DIVERGENCE; INNOVATION; LEAST SQUARES METHOD; LIFE HISTORY TRAIT; LOCOMOTION; MARINE ENVIRONMENT; MORPHOLOGY; MORPHOMETRY; PHENOTYPE; PHYLOGENETICS; TELEOST;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; EVOLUTION; FIN (ORGAN); GENETICS; HISTOLOGY; LOCOMOTION; PHYLOGENY; PHYSIOLOGY; TETRAODONTIFORMES;

ANIMAL FINS; ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BODY SIZE; LOCOMOTION; MODELS, GENETIC; PHYLOGENY; TETRAODONTIFORMES;

BALISTIDAE; TETRAODONTIFORMES; VERTEBRATA;

EID: 79959956893     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01275.x     Document Type: Article

References (103)

1. Adams, D., F. L. Rohlf, and D. Slice 2004. Geometric morphometrics: ten years of progress following the 'revolution'. Ital. J. Zool. 71:5-16.
2. Akaike, H. 1973. Information theory as an extension of the maximum likelihood principle. Pp. 267-281 in B. N. Petrov and F. Csaki, eds. Second annual symposium on information theory. Akademi Kiado, Budapest
3. Alesandrini, S., and G. Bernardi 1999. Ancient species flocks and recent speciation events: what can rockfish teach us about cichlids (and vice versa)? J. Mol. Evol. 49:814-818.
4. Alfaro, M. E., C. D. Brock, and F. Santini 2007. Do reefs drive diversification in marine fish? Examples from the pufferfishes and their allies. Evolution 61:2104-2126.
5. Alfaro, M. E., C. D. Brock, B. Banbury, and P. C. Wainwright 2009a. Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fish? BMC Evol. Biol. 9:255.
6. Alfaro, M. E., F. Santini, C. D. Brock, H. Alamillo, A. Dornburg, D. L. Rabosky, G. Carnevale, and L. J. Harmon 2009b. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl. Acad. Sci. USA 32:13410-13414.
7. Bannikov, A. F., and J. C. Tyler 2008. A new genus and species of triggerfish from the middle Eocene of the northern Caucasus, the earliest member of the balistidae (Tetraodontiformes). Paleontol. J. 42:615-620.
8. Barbour, C. D. 1973. A biogeographical history of Chirostoma (Pisces: Atherinidae): a species flock from the Mexican Plateau. Copeia 1973:533-556.
9. Bean, K., G. P. Jones, and M. J. Caley 2002. Relationships among distribution, abundance, and microhabitat specialization in a guild of coral reef triggerfish (family Balistidae). Mar. Ecol-Prog. Ser. 233:263-272.
10. Bellwood, D. R., P. C. Wainwright, C. J. Fulton, and A. S. Hoey 2006. Functional versatility supports coral reef biodiversity. Proc. R. Soc. Lond. B 273:101-107.
11. Blomberg, S., T. Garland, and A. Ives 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745.
12. Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge Univ. Press, Cambridge, UK
13. Bookstein, F. L. 1997. Morphometric tools for landmark data: geometry and biology. Cambridge Univ. Press, Cambridge, UK
14. Bookstein, F. L., and F. J. Rohlf 2004. From "mathematical dissection of anatomies" to morphometrics: a twenty-first-century appreciation of Charles Oxnard. Pp. 378-390 in F. Anapol, R. Z. German, and N. G. Jablonski, eds. Shaping primate evolution: form, function, and behavior. Cambridge Univ. Press, Cambridge
15. Brandley, M., A. Schmitz, and T. W. Reeder 2005. Partitioned Bayesian analyses, partition choice, and phylogenetic relationships of scincid lizards. Syst. Biol. 54:373-390.
16. Brock, C. D., L. J. Harmon, M. E. Alfaro 2011. Testing for temporal variation in diversification rates when sampling is incomplete and nonrandom. Syst. Biol. In press
17. Brown, J., and A. Lemmon 2007. The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. Syst. Biol. 56:643-655.
18. Budd, A. F., and J. M. Pandolfi 2010. Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328:1558-1561.
19. Burnham, K. P., and D. R. Anderson 2002. Model selection and multimodel inference, a practical information-theoretic approach. Springer, New York
20. Collar, D. C., P. C. Wainwright, and M. E. Alfaro 2008. Integrated diversification of locomotion and feeding in labrid fishes. Biol. Lett. 4:84-86.
21. Cusimano, N., and S. S. Renner 2010. Slowdowns in diversification rates from real phylogenies may not be real. Syst. Biol. 59:458-464.
22. Dabiri, J. O. 2009. Optimal vortex formation as a unifying principle in biological propulsion. Ann. Rev. Fluid Mech. 41:17-33.
23. Day, J. J., and M. Wilkinson 2006. On the origin of the Synodontis catfish species flock from Lake Tanganyika. Biol. Letts. 2:548-552.
24. Dornburg, A., F. Santini, and M. Alfaro 2008. The influence of model averaging on clade posteriors: an example using the triggerfishes (family balistidae). Syst. Biol. 57:905-919.
25. Drummond, A. J., S. Y. W. Ho, M. J. Phillips, and A. Rambaut 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
26. Dyreson, E., and D. R. Maddison 2003. Rhetenor package for morphometrics for the Mesquite System. version 1.0. Available at (accessed August 24, 2008).
27. Eble, G. 2000. Contrasting evolutionary flexibility in sister groups: disparity and diversity in Mesozoic atelostomate echnoids. Paleobiology 26:56-79.
28. Eschmeyer, W. N. ed. 2010. Catalog of Fishes electronic version. 2010 Available at (accessed October 25, 2010).
29. Foote, M. 1997. The evolution of morphological diversity. Annu. Rev. Ecol. Syst. 28:129-152.
30. Freckleton, R., and P. Harvey 2006. Detecting non-Brownian trait evolution in adaptive radiations. PLoS Biol. 4:e373.
31. Fulton, C. J., D. R. Bellwood, and P. C. Wainwright 2005. Wave energy and swimming performance shape coral reef fish assemblages. Proc. R. Soc. Lond. B 272:827-832.
32. Gavrilets, S., and J. B. Losos 2009. Adaptive radiation: contrasting theory with data. Science 323:732-737.
33. Harmon, L. J., J. A. Schulte, J. B. Losos, and A. Larson 2003. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301:961-964.
34. Harmon, L., J. Weir, C. D. Brock, and W. Challenger 2007. GEIGER: investigating evolutionary radiations. Bioinformatics 24:129-131.
35. Harmon, L. J., J. B. Losos, J. Davies, R. G. Gillespie, J. L. Gittleman, W. B. Jennings, K. Kozak, M. A. McPeek, F. Moreno-Roark, and T. J. Near 2010. Early bursts of body size and shape evolution are rare in comparative data. Evolution 64:2385-2396.
36. Higham, T. E. 2007. The integration of locomotion and prey capture in vertebrates: morphology, behavior, and performance. Integr. Comp. Biol. 47:82-91.
37. Holcroft, N. I. 2005. A molecular analysis of the interrelationships of tetraodontiform fishes (Acanthomorpha: Tetraodontiformes). Mol. Phylogenet. Evol. 34:525-544.
38. Hunt, D. M., J. Fitzgibbon, S. J. Slobodyanyuk, J. K. Bowmaker, and K. S. Dulai 1997. Molecular evolution of the cottoid fish endemic to Lake Baikal deduced from nuclear DNA evidence. Mol. Phylogenet. Evol. 8:415-422.
39. Jablonski, D. 2005. Evolutionary innovations in the fossil record: the intersection of ecology, development and macroevolution. J. Exp. Zool. B 304B:504-519.
40. Johnson, M. A., L. J. Revell, and J. B. Losos 2009. Behavioral covergence and adaptive radiation: effects of habitat use on territorial behavior in Anolis lizards. Evolution 64:1151-1159.
41. Kass, R. E., and A. E. Raftery 1995. Bayes factors. J. Am. Stat. Assoc. 90:773-795.
42. Klingenberg, C. P. 2008. MorphoJ. Faculty of Life Sciences, University of Manchester, UK. Available at (accessed August 24, 2008).
43. Korsmeyer, K. E., J. F. Steffensen, and J. Herksin 2002. Energetics of median and paired fin swimming, body, and caudal fin swimming, and gait transition in parrotfish (Scarus schlegeli) and triggerfish (Rhinecanthus aculeatus). J. Exp. Biol. 205:1253-1263.
44. Lauder, G. V., and P. G. A. Madden 2006. Learning from fish: kinematics and experimental hydrodynamics for roboticists. Int. J. Automat. Comput. 4:325-335.
45. Lauder, G. V. 2010. Swimming hydrodynamics: ten questions and the technical approaches needed to solve them. Anim. Locom. 1:3-15.
46. Lieske, E., and R. Myers 2001. Coral reef fishes. Princeton Univ. Press, Princeton, NJ
47. Lighthill, J., and R. Blake 1990a. Biofluiddynamics of balistiform and gymnotiform locomotion. Part 1. Biological background, and analysis by elongated-body theory. J. Fluid Mech. 212:183-207.
48. Lighthill, J., and R. Blake 1990b. Biofluiddynamics of balistiform and gymnotiform locomotion. Part 2. The pressure distribution arising in two-dimensional irrotational flow from a general symmetrical motion of a flexible flat plate normal to itself. J. Fluid Mech. 213:1-10.
49. Lighthill, J., and R. Blake 1990c. Biofluiddynamics of balistiform and gymnotiform locomotion. Part 3. Momentum enhancement in the presence of a body of elliptic cross-section. J. Fluid Mech 213:11-20.
50. Lighthill, J., and R. Blake 1990d. Biofluiddynamics of balistiform and gymnotiform locomotion. Part 4. Short-wavelength limitation on momentum enhancement. J. Fluid Mech. 213:21-28.
51. Losos, J. B. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Univ. of California Press, Berkeley, CA
52. Loofbourrow, H. 2009. Hydrodynamics of balistiform swimming in the Picasso triggerfish, Rhinecanthus aculeatus. Masters thesis. Univ. of British Columbia, Vancouver
53. Mabee, P. M., P. L. Crotwell, N. C. Bird, and A. C. Burke 2002. Evolution of median fin modules in the axial skeleton of fishes. J. Exp. Zool. 294:77-90.
54. Maddison, W., and D. Maddison 2008. Mesquite: a modular system for evolutionary analysis. Version 2.5.
55. Mittal, R., H. Dong, M. Bozkurttas, G. V. Lauder, and P. G. A. Madden 2006. Locomotion with flexible propulsors II: computational modeling and analysis of pectoral fin swimming in sunfish. Bioinsp. Biomimet. 1:S35-S41.
56. Monteiro, L. 1999. Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol. 48:192-199.
57. Nylander, J. A. A., J. C. Wilgenbusch, D. L. Warren, and D. L. Swofford 2008. AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581-583.
58. Palumbi, S. R. 1994. Genetic Divergence, Reproductive Isolation, and Marine Speciation. Annu. Rev. Ecol. Syst. 25:547-572.
59. Paradis, E., J. Claude, and K. Strimmer 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
60. Posada, D., and K. A. Crandall 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics (Oxford) 14:817-8.
61. Price, T. D. 2010. The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus). Phil. Trans. R. Soc. B 365:1749-1762.
62. Pybus, O. G., and P. H. Harvey 2000. Testing macro-evolutionary models using incomplete molecular phylogenies. Philos. Trans. R. Soc. Lond. B 267:2267-2272.
63. Quental, T. B., and C. R. Marshall 2009. Extinction during evolutionary radiations: reconciling the fossil record with molecular phylogenies. Evolution 63:3158-3167.
64. Rabosky, D. L. 2006a. Likelihood methods for detecting temporal shifts in diversification rates. Evolution 60:1152-1164.
65. Rabosky, D. L. 2006b. LASER: a maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evol. Bioinform. Online 2:257-260.
66. Rabosky, D., and I. Lovette 2006a. Density-dependent diversification in North American wood warblers. Proc. R. Soc. Lond. B. 275:2363-2371.
67. Rabosky, D., S. Donnellan, A. Talaba, and I. Lovette 2007. Exceptional among-lineage variation in diversification rates during the radiation of Australia's largest vertebrate clade. Proc. R. Soc. Lond. B 274:2915-2923.
68. Rabosky, D., S. Donnellan, A. Talaba, and I. Lovette 2006b. Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution 62:1866-1875.
69. Rabosky, D. L. 2009. Heritability of extinction rates links diversification patterns in molecular phylogenies and the fossil record. Syst. Biol. 58:629-640.
70. Raup, D. M. 1985. Mathematical models of cladogenesis. Paleobiology 11:42-52.
71. Rice, A. R., and M. W. Westneat 2005. Coordination of feeding, locomotor and visual systems in parrotfishes (Teleostei: Labridae). J. Exp. Biol. 208, 3503-3518.
72. Rocha, L. A., and B. W. Bowen 2008. Speciation in coral reef fishes. J. Fish Biol. 72:1101-1121.
73. Rohlf, F., and D. Slice 1990. Extensions of the procrustes method for the optimal superimposition of landmarks. Syst. Zool 39:40-59.
74. Rohlf, F. J. 1993. "Relative Warp Analysis and an Example of its Application to Mosquito Wings." Pp. 132-159 in L. F. Marcus, E. Bello, and A. Garcia-Valdecasas, eds. Contributions to morphometrics. Museo Nacional de Ciencias Naturales, Madrid
75. Rohlf, F. J. 2003. Bias and error in estimates of mean shape in morphometrics. J. Hum. Evol. 44:665-683.
76. Rohlf, F. J. 2005. Geometric morphometrics simplified. Review of "Geometric Morphometrics for Biologists: a primer. Trends Ecol. Evol. 20:13-14.
77. Rohlf, F. J. 2006. TPS series. Department of Ecology and Evolution, State University of New York, Stony Brook, NY Available at
78. Rohlf, F. J. 2007. TPS software series. Department of Ecology and Evolution, State University of New York, Stony Brook.
79. Rohlf, F. J., and M. Corti 2000. The use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49:740-753.
80. Santini, F., and J. C. Tyler 2003. A phylogeny of the families of fossil and extant tetraodontiform fishes (Acanthomorpha, Tetraodontiformes), Upper Cretaceous to recent. Zool. J. Linn. Soc. 139:565-617.
81. Santini, F., and J. C. Tyler 2004. The importance of even highly incomplete fossil taxa in reconstructing the phylogenetic relationships of the Tetraodontiformes (Acanthomorpha: Pisces). Integr. Comp. Biol. 44:349-357.
82. Santini F., L. J. Harmon, G. Carnevale, and M. E. Alfaro 2009. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol. Biol. 9:194.
83. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, Oxford
84. Schultz, O. 2004. A triggerfish (Osteichthyes: Balistidae: Balistes) from the Badenian (Middle Miocene) of the VIenna and the Styrian Basin (Central Paratethys). Annalen des Naturhistorischen Museums in Wien 106 A:345-369.
85. Seehausen, O. 2002. Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14600 year history for its cichlid species flock. Proc. R. Soc. Lond. B 269:491-497.
86. Seehausen, O. 2006. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. B 273:1987-1998.
87. Sfakiotakis, M., D. Lane, and J. Davies 1999. Review of Fish Swimming modes for aquatic locomotion. IEEE J. Oceanic Eng. 24:237-252.
88. Sidlauskas, B. 2007. Testing for unequal rates of morphological diversification in the absence of a detailed phylogeny: a case study from characiform fishes. Evolution 61:299-316.
89. Sidlauskas, B. 2008. Continuous and arrested morphological diversification in sister clades of characiform fish: a phylomorphospace approach. Evolution 62:3135-3156.
90. Slater, G. J., S. A. Price, F. Santini, and M. E. Alfaro 2010. Diversity versus disparity and the radiation of modern cetaceans. Proc. R. Soc. Lond. B 277:3097.
91. Sorenson, L. 2007. Examining morphological characteristics of triggerfish: a three-dimensional reconstruction of skeletal and muscular features of Rhinecanthus rectangulus. J. Young Investigators 16:3.
92. Tyler, J. C., and F. Santini 2002. Review and reconstruction of the tetraodontiform fishes from the Eocene of Monte Bolca, Italy, with comments on related Tertiary taxa. Studi e Rieche sui Giacimenti Terziari di Bolca, Museo Civico di Storia Naturale di Verona 9:47-119.
93. Tytell, E. D. 2006. Median fin function in bluegill sunfish, Lepomis macrochirus: streamwise vortex structure during steady swimming. J. Exp. Biol. 209:1516-1534.
94. Valentine, J. W., and D. Jablonski 2003. Morphological and developmental macroevolution: a paleontological perspective. Int. J. Dev. Biol. 47:517-522.
95. Villier, L., and G. Eble 2004. Assessing the robustness of disparity estimates: the impact of morphometric scheme, temporal scale, and taxonomic level in spatangoid echinoids. Paleobiology 30:652-665.
96. Walker, J. A., and M. W. Westneat 2002. Performance limits of labriform propulsion and correlates with fin shape and motion. J. Exp. Biol. 205:177-187.
97. Witte, F. 1984. Ecological differentiation in Lake Victoria haplochromines: comparison of cichlid species flocks in African lakes. Pp. 155-167 in A. A. Echelle and I. Kornfield, eds. Evolution of fish species flocks. Univ. of Maine at Orono Press, Orono
98. Wright, B. 2000. Form and function in aquatic flapping propulsion: morphology, kinematics, hydrodynamics, and performance of the triggerfishes (Tetraodontiformes: balistidae). Ph.D. thesis. University of Chicago, Chicago
99. Yamanoue, Y., M. Miya, K. Matsuura, H. Sakai, M. Katoh, and M. Nishida 2008. Unique patterns of pelvic fin evolution: a case study of balistoid fishes (Pisces: Tetraodontiforms) based on whole mitochondrial genome sequences. Mol. Phylogenet. Evol. 50:179-189.
100. Yang, Z., and B. Rannala 2006. Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol. Biol. Evol. 23:212-226.
101. Yoder, J. B., S. DesRoches, J. M. Eastman, L. Gentry, W. K. W. Godsoe, T. Hagey, D. Jochimsen, B. P. Oswald, J. Robertson, B. A. J. Sarver, et al. 2010. Ecological opportunity and the origin of adaptive radiations. J. Evol. Biol. 23:1581-1596.
102. Zelditch, M., H. Sheets, and W. Fink 2000. Spatiotemporal reorganization of growth rates in the evolution of ontogeny. Evolution 54:1363-1371.
103. Zelditch, M., D. Swiderski, D. Sheets, and W. Fink 2004. Geometric morphometrics for biologists: a primer. Elsevier Acad. Press, San Diego, CA