Evolutionary Biology

, Volume 42, Issue 3, pp 283–295 | Cite as

Body Shape Evolution in Sunfishes: Divergent Paths to Accelerated Rates of Speciation in the Centrarchidae

  • Andrew J. Smith
  • Nathan Nelson-Maney
  • Kevin J. Parsons
  • W. James Cooper
  • R. Craig Albertson
Research Article


Vertebrate evolutionary radiations are the result of divergence along a variety of ecological and behavioural axes. In addition, the potential for clades to evolve along any one axis can be strongly influenced by the types and levels of phenotypic variation that are exposed to natural selection. Understanding the factors that promote and constrain morphological diversification is a central goal of evolutionary biology. Here we use the sunfishes (Centrarchidae), a perciform family containing three main clades (Lepomis, Micropterus, and a basal clade), to explore this question with respect to variation in body shape. We gathered morphological data from 26 of the 38 centrarchid species using geometric morphometrics and analyzed the resultant shape data over a time-calibrated phylogenetic tree. We find that centrarchids partitioned body shape early in their evolutionary history, a pattern that is largely associated with expansion into divergent foraging niches and elaboration of sexual ornamentation. The morphological disparity of each clade was tightly linked to integration: those clades with high disparity (Lepomis, basal clade) were the least integrated, while the opposite trend was observed in Micropterus. We also find evidence for an increase in speciation rate at the node leading to Lepomis and Micropterus, and a decline in speciation for the basal clade. Our data lead us to suggest different hypotheses for explaining accelerated speciation in Micropterus and Lepomis: invasion of a novel pursuit-predator niche that reduced resource competition (Micropterus), and the elaboration of opercular morphology (Lepomis), a trait that is linked to reproductive behaviour and facilitates mate recognition in communities with many sunfish species.


Freshwater fish Integration Disparity Geometric morphometrics Phylogenetic methods 



The authors wish to thank the Katherine Doyle (UMass, Amherst) and Caleb McMahan (Chicago Field Museum) for access to specimens. Thanks to Israel Del Toro and Benjamin Allen Concannon Smith for providing live centrarchid images. We also wish to acknowledge Elizabeth Dumont and an anonymous reviewer for comments and discussion on early versions of the manuscript. This work was funded by an OEB research grant awarded to A.J.S, the Department of Biology at UMass, Amherst, start-up funding from WSU to W.J.C, and from Glasgow University to K.J.P.

Supplementary material

11692_2015_9322_MOESM1_ESM.xlsx (63 kb)
Supplementary material 1 (XLSX 62 kb)


  1. Adams, D. C., Cardini, A., Monteiro, L. R., O’Higgins, P., & Rohlf, F. J. (2011). Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters. Journal of Human Evolution, 60(2), 240–243. doi: 10.1016/j.jhevol.2010.02.003.CrossRefPubMedGoogle Scholar
  2. Albertson, R. C., & Kocher, T. D. (2006). Genetic and developmental basis of cichlid trophic diversity. Heredity, 97(3), 211–221. doi: 10.1038/sj.hdy.6800864.CrossRefPubMedGoogle Scholar
  3. Alfaro, M. E., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D. L., et al. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 106(32), 13410–13414. doi: 10.1073/pnas.0811087106.PubMedCentralCrossRefPubMedGoogle Scholar
  4. Baker, W. H., Blanton, R. E., & Johnston, C. E. (2013). Diversity within the Redeye Bass, Micropterus coosae (Perciformes: Centrarchidae) species group, with descriptions of four new species. Zootaxa, 3635(4), 379–401.CrossRefPubMedGoogle Scholar
  5. Baker, W., Johnston, C., & Folkerts, G. (2008). The Alabama bass, Micropterus henshalli (Teleostei: Centrarchidae), from the Mobile River basin. Zootaxa, 67, 57–67.Google Scholar
  6. Bollback, J. P. (2006). SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics, 7, 88. doi: 10.1186/1471-2105-7-88.PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bolnick, D. I. (2009). Hybridization and speciation in centrarchids. In S. J. Cooke & D. P. Phillip (Eds.), Centrarchid fishes: diversity, biology and conservation (pp. 39–69). Chichester, UK: Wiley.CrossRefGoogle Scholar
  8. Bolnick, D. I., & Near, T. J. (2005). Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution, 59(8), 1754–1767.CrossRefPubMedGoogle Scholar
  9. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference : A practical information-theoretic approach (2nd ed., p. 488). New York, NY: Springer.Google Scholar
  10. Clavel, J., King, A., & Paradis, E. (2014). mvMORPH: Multivariate comparative tools for fitting evolutionary models to morphometric data (Version 1.0.2).
  11. Collar, D. C., Near, T. J., & Wainwright, P. C. (2005). Comparative analysis of morphological diversity: Does disparity accumulate at the same rate in two lineages of centrarchid fishes? Evolution, 59(8), 1783–1794.CrossRefPubMedGoogle Scholar
  12. Collar, D. C., O’Meara, B. C., Wainwright, P. C., & Near, T. J. (2009). Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution, 63(6), 1557–1573. doi: 10.1111/j.1558-5646.2009.00626.x.CrossRefPubMedGoogle Scholar
  13. Collar, D. C., & Wainwright, P. C. (2006). Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution, 60(12), 2575–2584.CrossRefPubMedGoogle Scholar
  14. Cooper, W. J., Parsons, K., McIntyre, A., Kern, B., McGee-Moore, A., & Albertson, R. C. (2010). Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLoS One, 5(3), e9551. doi: 10.1371/journal.pone.0009551.PubMedCentralCrossRefPubMedGoogle Scholar
  15. Cooper, W. J., Wernle, J., Mann, K., & Albertson, R. C. (2011). Functional and genetic integration in the skulls of lake malawi cichlids. Evolutionary Biology, 38(3), 316–334. doi: 10.1007/s11692-011-9124-9.CrossRefGoogle Scholar
  16. Cooper, W. J., & Westneat, M. W. (2009). Form and function of damselfish skulls: Rapid and repeated evolution into a limited number of trophic niches. BMC evolutionary biology, 9(1), 24.PubMedCentralCrossRefPubMedGoogle Scholar
  17. Darwin, C. R. (1859). On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life (p. 502). London, UK: John Murray.Google Scholar
  18. Foote, M. (1993). Contributions of individual taxa to overall morphological disparity. Paleobiology, 19(4), 403–419.Google Scholar
  19. Frédérich, B., Sorenson, L., Santini, F., Slater, G. J., & Alfaro, M. E. (2013). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). The American Naturalist, 181(1), 94–113. doi: 10.1086/668599.CrossRefPubMedGoogle Scholar
  20. Gavrilets, S., & Losos, J. B. (2009). Adaptive radiation: Contrasting theory with data. Science, 323(5915), 732–737. doi: 10.1126/science.1157966.CrossRefPubMedGoogle Scholar
  21. Goddard, K., & Mathis, A. (1997). Do opercular flaps of male longear sunfish (Lepomis megalotis) serve as sexual ornaments during female mate choice? Ethology Ecology and Evolution, 9, 223–231.CrossRefGoogle Scholar
  22. Goddard, K., & Mathis, A. (2000). Opercular flaps as sexual ornaments for male longear sunfish (Lepomis megalotis): Male condition and male–male competition. Ethology, 106, 631–643.CrossRefGoogle Scholar
  23. Goswami, A., Smaers, J. B., Soligo, C., & Polly, P. D. (2014). The macroevolutionary consequences of phenotypic integration: From development to deep time. Philosophical Transactions of the Royal Society B: Biological Sciences, 369, 20130254.CrossRefGoogle Scholar
  24. Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., & Marcucio, R. S. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology,. doi: 10.1007/s11692-009-9076-5.PubMedCentralPubMedGoogle Scholar
  25. Hansen, T. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems, 69, 83–94.CrossRefPubMedGoogle Scholar
  26. Harmon, L. J., Losos, J. B., Jonathan Davies, T., Gillespie, R. G., Gittleman, J. L., Bryan Jennings, W., et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64(8), 2385–2396. doi: 10.1111/j.1558-5646.2010.01025.x.PubMedGoogle Scholar
  27. Harmon, L. J., Schulte, J. A., Larson, A., & Losos, J. B. (2003). Tempo and mode of evolutionary radiation in iguanian lizards. Science, 301, 961–964. doi: 10.1126/science.1084786.CrossRefPubMedGoogle Scholar
  28. Hipsley, C. A., Miles, D. B., Müller, J., & Mu, J. (2014). Morphological disparity opposes latitudinal diversity gradient in lacertid lizards. Biology Letters, 10(5), 20140101.PubMedCentralCrossRefPubMedGoogle Scholar
  29. Hodgson, J. R., He, X., Schindler, D. E., & Kitchell, J. F. (1997). Diet overlap in a piscivore community. Ecology of Freshwater Fish, 6, 144–149.CrossRefGoogle Scholar
  30. Holzman, R., Day, S. W., Mehta, R. S., & Wainwright, P. C. (2008). Integrating the determinants of suction feeding performance in centrarchid fishes. The Journal of experimental biology, 211(20), 3296–3305. doi: 10.1242/jeb.020909.CrossRefPubMedGoogle Scholar
  31. Hu, Y., Parsons, K., & Albertson, R. C. (2014). Evolvability of the cichlid jaw: New tools provide insights into the genetic basis of phenotypic integration. Evolutionary Biology, 41(1), 145–153. doi: 10.1007/s11692-013-9254-3.Google Scholar
  32. Keenleyside, M. H. A. (1967). Behavior of male sunfishes (genus Lepomis) towards females of three species. Evolution, 21, 688–695.CrossRefGoogle Scholar
  33. Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635. doi: 10.1038/nrg2829.PubMedGoogle Scholar
  34. Kocher, T. D. (2004). Adaptive evolution and explosive speciation: The cichlid fish model. Nature Reviews Genetics, 5(4), 288–298. doi: 10.1038/nrg1316.CrossRefPubMedGoogle Scholar
  35. Lerner, H. R. L., Meyer, M., James, H. F., Hofreiter, M., & Fleischer, R. C. (2011). Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers. Current biology: CB, 21(21), 1838–1844. doi: 10.1016/j.cub.2011.09.039.CrossRefPubMedGoogle Scholar
  36. Losos, J. B. (1998). Contingency and determinism in replicated adaptive radiations of Island Lizards. Science, 279(5359), 2115–2118. doi: 10.1126/science.279.5359.2115.CrossRefPubMedGoogle Scholar
  37. Losos, J. B. (2010). Adaptive radiation, ecological opportunity, and evolutionary determinism. American Society of Naturalists E. O. Wilson award address. The American Naturalist, 175(6), 623–639. doi: 10.1086/652433.CrossRefPubMedGoogle Scholar
  38. Maan, M. E., & Seehausen, O. (2011). Ecology, sexual selection and speciation. Ecology Letters, 14(6), 591–602. doi: 10.1111/j.1461-0248.2011.01606.x.CrossRefPubMedGoogle Scholar
  39. Manly, B. F. J. (1997). Randomization, bootstrap and Monte Carlo methods in biology (2nd ed., p. 480). London, UK: Chapman and Hall.Google Scholar
  40. Matthews, B., Marchinko, K. B., Bolnick, D. I., & Mazumder, A. (2010). Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation. Ecology, 91(4), 1025–1034.CrossRefPubMedGoogle Scholar
  41. Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22(24), 2362–2368. doi: 10.1016/j.cub.2012.10.048.CrossRefPubMedGoogle Scholar
  42. Muschick, M., Nosil, P., Roesti, M., Dittmann, M. T., Harmon, L., & Salzburger, W. (2014). Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika. Proceedings of the Royal Society B: Biological Sciences, 281, 1795. doi: 10.1098/rspb.2014.0605.CrossRefGoogle Scholar
  43. Near, T. J., Bolnick, D. I., & Wainwright, P. C. (2005). Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution, 59(8), 1768–1782.CrossRefPubMedGoogle Scholar
  44. Near, T., Kassler, T., & Koppelman, J. (2003). Speciation in North American Black Basses, Micropterus (Actinopterygii: Centrarchidae). Evolution, 57(7), 1610–1621.CrossRefPubMedGoogle Scholar
  45. Neff, B. D. (2004). Stabilizing selection on genomic divergence in a wild fish population. Proceedings of the National Academy of Sciences of the United States of America, 101(8), 2381–2385.PubMedCentralCrossRefPubMedGoogle Scholar
  46. Norton, S. F., & Brainerd, E. L. (1993). Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. Journal of Experimental Biology, 176, 11–29.Google Scholar
  47. Nylin, S., & Wahlberg, N. (2008). Does plasticity drive speciation? Host-plant shifts and diversification in nymphaline butterflies (Lepidoptera: Nymphalidae) during the tertiary. Biological Journal of the Linnean Society, 94(1), 115–130. doi: 10.1111/j.1095-8312.2008.00964.x.CrossRefGoogle Scholar
  48. Parsons, K. J., Márquez, E., & Albertson, R. C. (2012). Constraint and opportunity: The genetic basis and evolution of modularity in the cichlid mandible. The American Naturalist, 179(1), 64–78. doi: 10.1086/663200.CrossRefPubMedGoogle Scholar
  49. Parsons, K. J., & Robinson, B. W. (2006). Replicated evolution of integrated plastic responses during early adaptive divergence. Evolution, 60(4), 801–813.CrossRefPubMedGoogle Scholar
  50. Pigliucci, M. (2008). Is evolvability evolvable? Nature Reviews Genetics, 9, 75–82. doi: 10.1038/nrg2278.CrossRefPubMedGoogle Scholar
  51. Polly, P. D., Lawing, A. M., Fabre, A.-C., & Goswami, A. (2013). Phylogenetic principal components analysis and geometric morphometrics. Hystrix, the Italian Journal of Mammalogy, 24(1), 33–41. doi: 10.4404/hystrix-24.1-6383.Google Scholar
  52. Rabosky, D. (2006). LASER: A maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evolutionary Bioinformatics Online, 2, 247–250.PubMedCentralGoogle Scholar
  53. Rabosky, D. L., & Lovette, I. J. (2008). Density-dependent diversification in North American wood warblers. Proceedings of the Royal Society B: Biological Sciences, 275(1649), 2363–2371. doi: 10.1098/rspb.2008.0630.PubMedCentralCrossRefPubMedGoogle Scholar
  54. Rabosky, D. L., Santini, F., Eastman, J., Smith, S. A., Sidlauskas, B., Chang, J., & Alfaro, M. E. (2013). Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications, 4, 1958. doi: 10.1038/ncomms2958.CrossRefPubMedGoogle Scholar
  55. Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223. doi: 10.1111/j.2041-210X.2011.00169.x.CrossRefGoogle Scholar
  56. Rohlf, F. J. (1998). On applications of geometric morphometrics to studies of ontogeny and phylogeny. Systematic Biology, 47, 147–167. doi: 10.1080/106351598261094.CrossRefPubMedGoogle Scholar
  57. Rohlf, F. J. (2004). TPS Software.
  58. Sidlauskas, B. (2008). Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution, 62, 3135–3156. doi: 10.1111/j.1558-5646.2008.00519.x.CrossRefPubMedGoogle Scholar
  59. Simpson, G. G. (1944). Tempo and mode in evolution (p. 237). New York, NY: Columbia University Press.Google Scholar
  60. Slater, G. J., Price, S. A., Santini, F., & Alfaro, M. E. (2010). Diversity versus disparity and the radiation of modern cetaceans. Proceedings of the Royal Society B: Biological Sciences, 277(1697), 3097–3104. doi: 10.1098/rspb.2010.0408.PubMedCentralCrossRefPubMedGoogle Scholar
  61. Smith, A. J., Rosario, M. V., Eiting, T. P., & Dumont, E. R. (2014). Joined At the Hip: Linked Characters and the Problem of Missing Data in Studies of Disparity. Evolution, 68(8), 2386–2400. doi: 10.1111/evo.12435.PubMedGoogle Scholar
  62. Streelman, J. T., Alfaro, M., Westneat, M. W., Bellwood, D. R., & Karl, Sa. (2002). Evolutionary history of the parrotfishes: biogeography, ecomorphology, and comparative diversity. Evolution, 56(5), 961–971.CrossRefPubMedGoogle Scholar
  63. Streelman, J. T., & Danley, P. D. (2003). The stages of vertebrate evolutionary radiation. Trends in Ecology & Evolution, 18(3), 126–131. doi: 10.1016/S0169-5347(02)00036-8.CrossRefGoogle Scholar
  64. Tobias, J. A., Montgomerie, R., & Lyon, B. E. (2012). The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philosophical Transactions of the Royal Society of London. Series B, Biological sciences, 367(1600), 2274–2293. doi: 10.1098/rstb.2011.0280.PubMedCentralCrossRefPubMedGoogle Scholar
  65. Wagner, C. E., Harmon, L. J., & Seehausen, O. (2012). Ecological opportunity and sexual selection together predict adaptive radiation. Nature, 487(7407), 366–369. doi: 10.1038/nature11144.CrossRefPubMedGoogle Scholar
  66. Warren, M. L, Jr. (2009). Centrarchid identification and natural history. In S. J. Cooke & D. P. Phillip (Eds.), Centrarchid fishes: Diversity, biology and conservation (pp. 375–535). Chichester, UK: Wiley.CrossRefGoogle Scholar
  67. Zachos, J. C., Dickens, G. R., & Zeebe, R. E. (2008). An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature, 451, 279–283. doi: 10.1038/nature06588.CrossRefPubMedGoogle Scholar
  68. Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer (2nd ed., p. 488). Waltham, MA: Academic Press.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Andrew J. Smith
    • 1
  • Nathan Nelson-Maney
    • 2
  • Kevin J. Parsons
    • 3
  • W. James Cooper
    • 4
  • R. Craig Albertson
    • 2
  1. 1.Graduate Program in Organismic and Evolutionary BiologyUniversity of MassachusettsAmherstUSA
  2. 2.Department of BiologyUniversity of MassachusettsAmherstUSA
  3. 3.Institute of Biodiversity, Animal Health and Comparative MedicineUniversity of GlasgowGlasgowUK
  4. 4.School of Biological SciencesWashington State UniversityPullmanUSA

Personalised recommendations