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

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Abstract

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.

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References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Bollback, J. P. (2006). SIMMAP: Stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics, 7, 88. doi:10.1186/1471-2105-7-88.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Bolnick, D. I., & Near, T. J. (2005). Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution, 59(8), 1754–1767.

    Article  PubMed  Google Scholar 

  • 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 

  • Clavel, J., King, A., & Paradis, E. (2014). mvMORPH: Multivariate comparative tools for fitting evolutionary models to morphometric data (Version 1.0.2). http://cran.r-project.org/package=mvMORPH.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 

  • Foote, M. (1993). Contributions of individual taxa to overall morphological disparity. Paleobiology, 19(4), 403–419.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gavrilets, S., & Losos, J. B. (2009). Adaptive radiation: Contrasting theory with data. Science, 323(5915), 732–737. doi:10.1126/science.1157966.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed Central  PubMed  Google Scholar 

  • Hansen, T. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems, 69, 83–94.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Keenleyside, M. H. A. (1967). Behavior of male sunfishes (genus Lepomis) towards females of three species. Evolution, 21, 688–695.

    Article  Google Scholar 

  • Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635. doi:10.1038/nrg2829.

    CAS  PubMed  Google Scholar 

  • Kocher, T. D. (2004). Adaptive evolution and explosive speciation: The cichlid fish model. Nature Reviews Genetics, 5(4), 288–298. doi:10.1038/nrg1316.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Manly, B. F. J. (1997). Randomization, bootstrap and Monte Carlo methods in biology (2nd ed., p. 480). London, UK: Chapman and Hall.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Near, T., Kassler, T., & Koppelman, J. (2003). Speciation in North American Black Basses, Micropterus (Actinopterygii: Centrarchidae). Evolution, 57(7), 1610–1621.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Parsons, K. J., & Robinson, B. W. (2006). Replicated evolution of integrated plastic responses during early adaptive divergence. Evolution, 60(4), 801–813.

    Article  PubMed  Google Scholar 

  • Pigliucci, M. (2008). Is evolvability evolvable? Nature Reviews Genetics, 9, 75–82. doi:10.1038/nrg2278.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Rabosky, D. (2006). LASER: A maximum likelihood toolkit for detecting temporal shifts in diversification rates from molecular phylogenies. Evolutionary Bioinformatics Online, 2, 247–250.

    PubMed Central  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rohlf, F. J. (1998). On applications of geometric morphometrics to studies of ontogeny and phylogeny. Systematic Biology, 47, 147–167. doi:10.1080/106351598261094.

    Article  CAS  PubMed  Google Scholar 

  • Rohlf, F. J. (2004). TPS Software. http://www.life.bio.sunysb.edu/morph/

  • 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.

    Article  PubMed  Google Scholar 

  • Simpson, G. G. (1944). Tempo and mode in evolution (p. 237). New York, NY: Columbia University Press.

    Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

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Acknowledgments

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.

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Authors and Affiliations

  1. Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA, 01003, USA

    Andrew J. Smith

  2. Department of Biology, University of Massachusetts, 221 Morrill Science Center, Amherst, MA, 01003, USA

    Nathan Nelson-Maney & R. Craig Albertson

  3. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, G12 8QQ, UK

    Kevin J. Parsons

  4. School of Biological Sciences, Washington State University, Pullman, WA, 99164, USA

    W. James Cooper

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  1. Andrew J. Smith
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Correspondence to Andrew J. Smith.

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Smith, A.J., Nelson-Maney, N., Parsons, K.J. et al. Body Shape Evolution in Sunfishes: Divergent Paths to Accelerated Rates of Speciation in the Centrarchidae. Evol Biol 42, 283–295 (2015). https://doi.org/10.1007/s11692-015-9322-y

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