Skip to main content
SpringerLink
Log in

Sympatric Divergence and Performance Trade-Offs of Bluegill Ecomorphs

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Phenotypic plasticity in response to environmental cues can create distinct morphological types within populations. This variation in form, and potentially function, may be a factor in initiating population divergence and the formation of new species. Here we show the translation of sympatric, habitat-specific morphological divergence into performance differences in energy economy, maneuverability and steady-state locomotion. Littoral and pelagic bluegill sunfish ecomorphs show differences in performance that appear adaptive within their respective habitats: greater maneuverability in the heavily vegetated littoral; greater steady-state swimming speed and economy in the open-water pelagic. This represents a trade-off in unsteady versus steady swimming performance, likely because morphological features associated with maximizing maneuverability are incompatible with enhancing steady-swimming performance. This may constrain the direction of adaptive change, maintaining the divergence created by phenotypic plasticity. The combination of habitat specific sympatric adaptation and constraints imposed by performance trade-offs may be an important factor underlying the high rate of speciation in freshwater fishes from post-glacial lakes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adolph, S. C., & Pickering, T. (2008). Estimating maximum performance: effects of intraindividual variation. Journal of Experimental Biology, 211, 1336–1343.

    Google Scholar 

  • Alfaro, M. E., Bolnick, D. I., & Wainwright, P. C. (2004). Evolutionary dynamics of complex biomechanical systems: An example using the four-bar mechanism. Evolution, 58, 495–503.

    PubMed  Google Scholar 

  • Arnold, S. J. (1983). Morphology, performance and fitness. American Zoologist, 23, 347–361.

    Google Scholar 

  • Arnold, S. J., & Bennett, A. F. (1988). Behavioural variation in natural populations. V. Morphological correlates of locomotion in the garter snake (Thamnophis radix). Biological Journal of the Linnean Society, 34, 175–190.

    Article  Google Scholar 

  • Bennett, A. F., Huey, R. B., & John-Alder, H. (1984). Physiological correlates of natural activity and locomotor capacity in two species of lacertid lizards. Journal of Comparative Physiology B, 154, 113–118.

    Article  Google Scholar 

  • Bernatchez, L., & Wilson, C. C. (1998). Comparative phylogeography of nearctic and palearctic freshwater fishes. Molecular Ecology, 7, 431–452.

    Article  Google Scholar 

  • Blake, R. W., Chatters, L. M., & Domenici, P. (1995). Turning radius of yellowfin tuna (Thunnus albacares) in unsteady swimming manoevres. Journal of Fish Biology, 46, 536–538.

    Article  Google Scholar 

  • Bolger, T., & Connolly, P. L. (1989). The selection of suitable indices for the measurement and analysis of fish condition. Journal of Fish Biology, 34, 171–182.

    Article  Google Scholar 

  • Bolnick, D. I., & Lau, O. L. (2008). Predictable patterns of disruptive selection in stickleback in postglacial lakes. The American Naturalist, 172(1), 1–11.

    Article  PubMed  Google Scholar 

  • Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board, Canada, 21, 1183–1226.

    Article  Google Scholar 

  • Brett, J. R., & Groves, T. D. D. (1979). Physiological energetics. In W. S. Hoar, D. J. Randall, & J. R. Brett (Eds.), Fish physiology (Vol. VIII, pp. 280–352). New York: Academic Press.

    Google Scholar 

  • Burgetz, I. J., Rojas-Vargas, A., Hinch, S. G., & Randall, D. J. (1998). Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology, 201, 2711–2721.

    PubMed  Google Scholar 

  • Calsbeek, R., & Irschick, D. J. (2007). The quick and the dead: Correlational selection on morphology, performance, and habitat use in island lizards. Evolution, 61(11), 2493–2503.

    Article  PubMed  Google Scholar 

  • Claireaux, G., Couturier, C., & Groison, A.-L. (2006). Effect of temperature on swimming speed and cost of transport in juvenile European sea bass. Journal of Experimental Biology, 209, 3420–3428.

    Article  PubMed  Google Scholar 

  • Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Ehrlbaum Associates.

    Google Scholar 

  • 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, 1783–1794.

    PubMed  Google Scholar 

  • Dadda, M., Koolhaus, W. H., & Domenici, P. (2010). Behavioural asymmetry affects escape performance in a teleost fish. Biology Letters, 6, 414–417.

    Article  PubMed  Google Scholar 

  • Darwin, C. (1859). On the origin of species. Murray: London.

    Google Scholar 

  • Domenici, P. (2003). Habitat, body design and the swimming performance of fish. In V. L. Bels, J.-P. Gasc, & A. Casinos (Eds.), Vertebrate biomechanics and evolution (pp. 137–160). Oxford, UK: BIOS Scientific Publishers Ltd.

    Google Scholar 

  • Ehlinger, T. J. (1989). Learning and individual variation in bluegill foraging: Habitat-specific techniques. Animal Behaviour, 38, 643–658.

    Article  Google Scholar 

  • Ehlinger, T. J. (1990). Habitat choice and phenotype-limited feeding efficiency in bluegill: Individual differences and trophic polymorphism. Ecology, 71(3), 886–896.

    Article  Google Scholar 

  • Ehlinger, T. J. (1991). Allometry and analysis of morphometric variation in the bluegill, Lepomis macrochirus. Copeia, 1991(2), 347–357.

    Article  Google Scholar 

  • Ehlinger, T. J., & Wilson, D. S. (1988). Complex foraging polymorphism in bluegill sunfish. Proceedings of the National Academy of Sciences, 85, 1878–1882.

    Article  CAS  Google Scholar 

  • Elstrott, J., & Irschick, D. J. (2004). Evolutionary correlations among morphology, habitat use and clinging performance in Caribbean Anolis lizards. Biological Journal of the Linnean Society, 83, 389–398.

    Article  Google Scholar 

  • Futuyma, D. J. (2010). Evolutionary constraint and ecological consequences. Evolution, 64, 1865–1884.

    Article  PubMed  Google Scholar 

  • Garland, T., Jr., Bennett, A. F., & Daniels, C. B. (1990). Heritability of locomotor performance and its correlates in a natural population. Experientia, 46, 530–533.

    Article  Google Scholar 

  • Garland, T., Jr., & Else, P. L. (1987). Seasonal, sexual and individual variation in endurance and activity metabolism in lizards. Regulatory, Integrative and Comparative Physiology, 252(3), R439–R449.

    CAS  Google Scholar 

  • Garland, T., Jr., & Kelly, S. A. (2006). Phenotypic plasticity and experimental evolution. Journal of Experimental Biology, 209, 2344–2361.

    Article  PubMed  Google Scholar 

  • Garland, T., Jr., & Losos, J. B. (1994). Ecological morphology of locomotor performance in squamate reptiles. Ecological Morphological Integrative Organismal Biology. Chicago: Univ. Chicago Press, pp. 240–302.

  • Gerry, S. P., Wang, J., & Ellerby, D. J. (2011). A new approach to quantifying morphological variation in bluegill sunfish Lepomis macrochirus. Journal of Fish Biology, 78, 1023–1034.

    Article  PubMed  CAS  Google Scholar 

  • Gerstner, C. (1999). Maneuverabilty of four species of coral-reef fish that differ in body and pectoral-fin morphology. Canadian Journal of Zoology, 77, 1102–1110.

    Article  Google Scholar 

  • Ghalambor, C. K., Walker, J. A., & Reznick, D. N. (2003). Multi-trait selection, adaptation, and constraints on the evolution of burst swimming performance. Integrative and Comparative Biology, 43, 431–438.

    Article  PubMed  Google Scholar 

  • Gross, M. R., & MacMillan, A. M. (1981). Predation and the evolution of colonial nesting in bluegill sunfish (Lepomis macrochirus). Behavioural Ecology and Sociobiology, 8, 163–174.

    Article  Google Scholar 

  • Huey, R. B., & Stevenson, R. D. (1979). Integrating thermal physiology and ecology of ectotherms: A discussion of approaches. American Zoologist, 19(1), 357–366.

    Google Scholar 

  • Jastrebski, C. J., & Robinson, B. W. (2004). Natural selection and the evolution of replicated trophic polymorphisms in pumpkinseed sunfish (Lepomis gibbosus). Evolutionary Ecology Research, 6, 285–305.

    Google Scholar 

  • Jones, E. A., Jong, A. S., & Ellerby, D. J. (2008). The effects of acute temperature change on swimming performance in bluegill sunfish Lepomis macrochirus. Journal of Experimental Biology, 211, 1386–1393.

    Article  PubMed  Google Scholar 

  • Jones, E. A., Lucey, K. S., & Ellerby, D. J. (2007). Efficiency of labriform swimming in the bluegill sunfish (Lepomis macrochirus). Journal of Experimental Biology, 210, 3422–3429.

    Article  PubMed  Google Scholar 

  • Kendall, J. L., Lucey, K. S., Jones, E. A., Wang, J., & Ellerby, D. J. (2007). Mechanical and energetic factors underlying gait transitions in bluegill sunfish (Lepomis macrochirus). Journal of Experimental Biology, 210, 4265–4271.

    Article  PubMed  Google Scholar 

  • Langerhans, R. B. (2009). Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. Journal of Evolutionary Biology, 22, 1057–1075.

    Article  PubMed  CAS  Google Scholar 

  • Langerhans, R. B., & Reznick, D. N. (2010). Ecology and evolution of swimming performance in fishes: Predicting evolution with biomechanics. In P. Domenici & B. G. Kapoor (Eds.), Fish locomotion: An etho-ecological perspective (pp. 200–248). Enfield: Science Publishers.

    Chapter  Google Scholar 

  • Losos, J. B., Walton, B. M., & Bennett, A. F. (1993). Trade-offs between sprinting and clinging ability in Kenyan chameleons. Functional Ecology, 7, 281–286.

    Article  Google Scholar 

  • Lurman, G. J., Bock, C. H., & Portner, H. O. (2007). An examination of the metabolic processes underpinning critical swimming in Atlantic cod (Gadus morhua L.) using in vivo 31P-NMR spectroscopy. Journal of Experimental Biology, 210, 3749–3756.

    Article  PubMed  CAS  Google Scholar 

  • Marras, S., Claireaux, G., McKenzie, D. J., & Nelson, J. A. (2010). Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. Journal of Experimental Biology, 213, 26–32.

    Article  PubMed  CAS  Google Scholar 

  • Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., et al. (1985). Developmental constraints and evolution. Quarterly Review of Biology, 6, 265–287.

    Google Scholar 

  • Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.

    Google Scholar 

  • Meyer, A. (1993) Trophic polymorphisms in cichlid fish: Do they represent intermediate steps during sympatric speciation and explain their rapid adaptive radiation? In: Schröder, J.-H. et al. (Eds.), New Trends in Ichthyology. Blackwell, pp. 257–266.

  • Mittelbach, G. S. (1981). Foraging efficiency and body size: A study of optimal diet and habitat use by bluegills. Ecology, 62, 1370–1386.

    Article  Google Scholar 

  • Norberg, U. M. (1995). How a long tail and changes in mass and wing shape affect the cost for flight in animals. Functional Ecology, 9, 48–54.

    Article  Google Scholar 

  • Papaj, D. R., & Prokopy, R. J. (1989). Ecological and evolutionary aspects of learning in phytophagous insects. Annual Review of Entomology, 34, 315–350.

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Parsons, K. J., & Robinson, B. W. (2007). Foraging performance of diet-induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism. Journal of Evolutionary Biology, 20, 673–684.

    Article  PubMed  CAS  Google Scholar 

  • Pettersson, L. B., & Hedenström, A. (2000). Energetics, cost reduction and functional consequences of fish morphology. Proceedings of the Royal Society of London B, 267, 759–764.

    Article  CAS  Google Scholar 

  • Pfennig, D. W. (1990). The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole. Oecologia, 85, 101–107.

    Article  Google Scholar 

  • Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. (2010). Phenotypic plasticity’s impacts on diversification and speciation. TREE, 25, 459–467.

    PubMed  Google Scholar 

  • Reidy, S. P., Kerr, S. R., & Nelson, J. A. (2000). Aerobic and anaerobic swimming performance of individual Atlantic cod. Journal of Experimental Biology, 203, 347–357.

    PubMed  CAS  Google Scholar 

  • Robinson, B. W. (2000). Trade-offs in habitat-specific foraging efficiency and the nascent adaptive divergence of sticklebacks in lakes. Behaviour, 137, 865–888.

    Article  Google Scholar 

  • Robinson, B. W., Wilson, D. S., Margosian, A. S., & Lotito, P. T. (1993). Ecological and morphological differentiation of pumpkinseed sunfish in lakes without bluegill sunfish. Evolutionary Ecology, 7, 451–464.

    Article  Google Scholar 

  • Robinson, B. W., Wilson, D. S., & Shea, G. O. (1996). Trade-offs of ecological specialization: An intraspecific comparison of pumpkinseed sunfish phenotypes. Ecology, 77(1), 170–178.

    Article  Google Scholar 

  • Rouleau, S., Glémet, H., & Magnan, P. (2009). Effects of morphology on swimming performance in wild and laboratory crosses of brook trout ecotypes. Functional Ecology, 24, 310–321.

    Article  Google Scholar 

  • Ryan, T. A. (1960). Significance tests for multiple comparison of proportions, variances and other statistics. Psychological Bulletin, 57, 318–328.

    Article  PubMed  CAS  Google Scholar 

  • Schluter, D. (1993). Adaptive radiation in sticklebacks: Size, shape, and habitat use efficiency. Ecology, 74, 699–709.

    Article  Google Scholar 

  • Schluter, D. (1995). Adaptive radiation in sticklebacks: Trade-offs in feeding performance and growth. Ecology, 76(1), 82–90.

    Article  Google Scholar 

  • Schluter, D. (1996). Ecological speciation in postglacial fishes. Philosophical Transactions of the Royal Society London B, 351, 807–814.

    Article  Google Scholar 

  • Schrank, A. J., & Webb, P. W. (1998). Do body and fin form affect the abilities of fish to stabilize swimming during maneuvers through vertical and horizontal tubes? Environmental Biology of Fishes, 53, 365–371.

    Article  Google Scholar 

  • Schrank, A. J., Webb, P. W., & Mayberry, S. (1999). How do body and paired-fin positions affect the ability of three teleost fishes to maneuver around bends? Canadian Journal of Zoology, 77, 203–210.

    Article  Google Scholar 

  • Schwenk, K. (2001). Functional units and their evolution. In G. P. Wagner (Ed.), The character concept in evolutionary biology (pp. 167–200). San Diego: Academic Press.

    Google Scholar 

  • Skúlason, S., & Smith, T. B. (1995). Resource polymorphisms in vertebrates. Trends in Ecology & Evolution, 10(9), 366–370.

    Article  Google Scholar 

  • Sorci, G., et al. (1995). Quantitative genetics of locomotor speed and endurance in the lizard. Lacerta vivipam Physiol Zool, 68, 698–720.

    Google Scholar 

  • Standen, E. M., & Lauder, G. V. (2005). Dorsal and anal fin function in bluegill sunfish (Lepomis macrochirus): Three-dimensional kinematics during propulsion and manoeuvring. Journal of Experimental Biology, 208, 2753–2763.

    Article  PubMed  CAS  Google Scholar 

  • Svanbäck, R., & Eklöv, P. (2003). Morphology dependent foraging efficiency in perch: A trade-off for ecological specialization? Oikos, 102(2), 273–284.

    Article  Google Scholar 

  • Taylor, E. B., & McPhail, J. D. (1986). Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Canadian Journal of Zoology, 64, 416–420.

    Article  Google Scholar 

  • Thomason, J. J. (1991). Cranial strength in relation to estimated biting forces in some mammals. Canadian Journal of Zoology, 69, 2326–2333.

    Article  Google Scholar 

  • Tytell, E. D., & Lauder, G. V. (2008). Hydrodynamics of the escape response in bluegill sunfish, Lepomis macrochirus. Journal of Experimental Biology, 211, 3359–3369.

    Article  PubMed  Google Scholar 

  • Tytell, E. D., Standen, E. M., & Lauder, G. V. (2008). Escaping Flatland: Three-dimensional kinematics and hydrodynamics of median fins in fishes. Journal of Experimental Biology, 211, 187–195.

    Article  PubMed  Google Scholar 

  • Vanhooydonck, B., Van Damme, R., & Aerts, P. (2001). Speed and stamina trade-off in lacertid lizards. Evolution, 55, 1040–1048.

    Article  PubMed  CAS  Google Scholar 

  • Walker, J. A. (1997). Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biological Journal of the Linnean Society, 61, 3–50.

    Google Scholar 

  • Walker, J. A. (1998). Estimating velocities and accelerations of animal locomotion: A simulation experiment comparing numerical differentiation algorithms. Journal of Experimental Biology, 201, 981–995.

    Google Scholar 

  • Walker, J. A. (2000). Does a rigid body limit maneuverability? Journal of Experimental Biology, 203, 3391–3396.

    PubMed  CAS  Google Scholar 

  • Walker, J. A. (2004). Dynamics of pectoral fin rowing in a fish with an extreme rowing stroke: The threespine stickleback (Gasterosteus aculeatus). Journal of Experimental Biology, 207, 1925–1939.

    Article  PubMed  Google Scholar 

  • Walker, J. A. (2007). A general model of functional constraints on phenotypic evolution. American Naturalist, 170, 681–689.

    Article  PubMed  Google Scholar 

  • Walker, J. A., & Westneat, M. W. (2000). Mechanical performance of aquatic rowing and flying. Proceedings of the Royal Society B, 267, 1875–1881.

    Article  PubMed  CAS  Google Scholar 

  • Walker, J. A., & Westneat, M. W. (2002). Performance limits of labriform propulsion and correlates with fin shape and motion. Journal of Experimental Biology, 205, 177–187.

    PubMed  Google Scholar 

  • Webb, P. W. (1984). Body form, locomotion and foraging in aquatic vertebrates. American Zoologist, 24, 107–120.

    Google Scholar 

  • Webb, P. W. (1992). Control of posture, depth, and swimming trajectories of fishes. Integrative and Comparative Biology, 42(1), 94–101.

    Article  Google Scholar 

  • Webb, P. W., LaLiberte, G. D., & Schrank, A. J. (1996). Does body and fin form affect the maneuverability of fish traversing vertical and horizontal slits? Environmental Biology of Fishes, 46, 7–14.

    Article  Google Scholar 

  • Wilson, D. S., Muzzall, P. M., & Ehlinger, T. J. (1996). Parasites, morphology and habitat use in a bluegill sunfish (Lepomis macrochirus) population. Copeia, 1996, 348–354.

  • Wund, M. A., Baker, J. A., Clancy, B., Golub, J. L., & Foster, S. A. (2008). A test of the ‘flexible stem’ model of evolution: Ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. American Naturalist, 172, 449–462.

    Article  PubMed  Google Scholar 

  • Yonekura, R., Kohmatsu, Y., & Yuma, M. (2007). Difference in the predation impact enhanced by morphological divergence between introduced fish populations. Biological Journal of the Linnean Society, 91, 601–610.

    Article  Google Scholar 

  • Yonekura, R., Nakai, K., & Yuma, M. (2002). Trophic polymorphism in introduced bluegill in Japan. Ecological Research, 17, 49–57.

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Kara Feilich, Cataia Ives and Jessica Liao for their assistance with these experiments. Funding for this project was provided by a Wellesley College Brachman-Hoffman grant to DJE and by NSF 0715937 to DJE.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA, 02481, USA

    David J. Ellerby

  2. Department of Biological Sciences, Fairfield University, 1073 North Benson Rd, Fairfield, CT, 06824, USA

    Shannon P. Gerry

Authors
  1. David J. Ellerby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shannon P. Gerry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David J. Ellerby.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ellerby, D.J., Gerry, S.P. Sympatric Divergence and Performance Trade-Offs of Bluegill Ecomorphs. Evol Biol 38, 422–433 (2011). https://doi.org/10.1007/s11692-011-9130-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-011-9130-y

Keywords

Search

Navigation