Skip to main content
SpringerLink
Log in

Genetic variation and phenotypic plasticity in a trophically polymorphic population of pumpkinseed sunfish (Lepomis gibbosus)

  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Summary

Adaptive variation can exist at a variety of scales in biological systems, including among species, among local populations of a single species and among individuals within a single population. Trophic or resource polymorphisms in fishes are a good example of the lowest level of this hierarchy. In lakes without bluegill sunfish (Lepomis macrochirus), pumpkinseed sunfish (Lepomis gibbosus) can be trophically polymorphic, including a planktivorous limnetic form found in the pelagic habitat, in addition to the usual benthic form found in the littoral zone. In this paper we examine the degree to which morphological differences between the two forms are caused by genetic differences versus phenotypic plasticity. Adults from pelagic and littoral sites in Paradox Lake, NY, were bred separately and their progeny were raised in cages both in the open water and shallow water habitats of an artificial pond. The experimental design permitted two tests of genetic differences between the breeding stocks (in open and shallow water cages, respectively) and two tests of phenotypic plasticity (in the limnetic and benthic offspring, respectively). Limnetic progeny were more fusiform than benthic progeny raised in the same habitat. In addition, progeny of both stocks displayed limnetic-type characteristics when raised in the open water and benthic-type characteristics in the shallow water. Thus, genetic differences and phenotypic plasticity both contributed to the trophic polymorphism. Phenotypic plasticity and genetic differentiation accounted for 53 and 14%, respectively, of the variation in morphology. This study addresses the nature of subtle phenotypic differences among individuals from a single population that is embedded within a complex community, a condition that is likely to be the norm for most natural populations, as opposed to very large differences that have evolved in relatively few populations that reside in species-poor environments.

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

Similar content being viewed by others

References

  • Baird, R.W., Abrams, P.A. and Dill, L. (1992) Possible indirect interactions between transient and resident killer whales: implications for the evolution of foraging specializations in the genusOrcinus.Oecologia 89 125–32.

    Google Scholar 

  • Behnke, R.J. (1972) The systematics of Salmonid fishes of recently glaciated lakes.J. Fish. Res. Bd Can. 29 639–71.

    Google Scholar 

  • Bentzen, P. and McPhail, J.D. (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair.Can. J. Zool. 62 2280–6.

    Google Scholar 

  • Boag, P.T. and Grant, P.R. (1981) Intense natural selection in a population of Darwin's finches (Geospizinae) in the Galapagos.Science 214 82–5.

    Google Scholar 

  • Bookstein, F., Chernoff, B., Elder, R., Humphries, J., Smith, G. and Strauss, R. (1985)Morphometrics in Evolutionary Biology. The Academy of Natural Sciences of Philadelphia, Philadelphia, PA.

    Google Scholar 

  • Bradshaw, A.D., NcNeilly, T.S. and Gregory, R.P.G. (1965) Industrialisation, evolution, and the development of heavy metal tolerance in plants. Ecology and the Industrial Society.Br. Ecol. Soc. Symp. 5 327–43.

    Google Scholar 

  • Brodie, E.D., III (1990) Genetics of the Garter's getaway.Nat. Hist. 7/90 45–50.

    Google Scholar 

  • Brönmark, C. and Miner, J.G. (1992) Predator-induced phenotypic change in body morpholgy in Crucian carp.Science 258 1348–50.

    Google Scholar 

  • Bull, J.J. (1987) Evolution of phenotypic variance.Evolution 41 303–15.

    Google Scholar 

  • Cheplick, G.P. (1991) A conceptual framework for the analysis of phenotypic plasticity and genetic contstraints in plants.Oikos 62 283–91.

    Google Scholar 

  • Collins, J.P. and Cheek, J.E. (1983) Effect of food and density on development of typical and cannibalistic salamander larvae inAmbystoma tigrinum nebulosum.Am. Zool. 23 77–84.

    Google Scholar 

  • Danzmann, R.G., Ferguson, M.M., Skulason, S., Snorrason, S.S. and Noakes, D.L.G. (1991) Mitochondrial DNA diversity among four sympatric morphs of Arctic charr,Salvelinus alpinus L., from Thingvallavatn, Iceland.J. Fish Biol. 39 649–60.

    Google Scholar 

  • Dominey, W.J. (1980) Female mimicry in male bluegill sunfish — genetic polymorphism?Nature 280 546–8.

    Google Scholar 

  • Ehlinger, T.J. (1991) Allometry and analysis of morphometric variation, in bluegill,Lepomis macrochirus.Copeia 1991 347–57.

    Google Scholar 

  • Ehrlich, P.R. and Raven, P.H. (1969) Differentiation of populations.Science 165 1228–32.

    PubMed  Google Scholar 

  • Endler, J.A. (1973) Gene flow and population differentiation.Science 179 243–50.

    PubMed  Google Scholar 

  • Endler, J.A. (1980) Natural selection on color patterns inPoecilia reticulata.Evolution 34 76–91.

    Google Scholar 

  • Endler, J.A. (1982) Convergent and divergent effects of natural selection on color patterns in two fish faunas.Evolution 36 178–88.

    Google Scholar 

  • Felley, J.D. and Avise, J.C. (1980) Genetic and morphological variation of bluegill populations in Florida lakes.Trans. Am. Fish. Soc. 109 108–15.

    Google Scholar 

  • Felley, J.D. and Smith, M.H. (1978) Phenotypic and genetic trends in bluegills of a single drainage.Copeia 1978 175–7.

    Google Scholar 

  • Ferguson, A. and Mason, F.M. (1981) Allozyme evidence for reproductively isolated sympatric populations of brown troutSalmo trutta L. in Lough Melvin, Ireland.J. Fish Biol. 18 629–42.

    Google Scholar 

  • Futuyma, D.J. and Moreno, G. (1988) The evolution of specialization.Ann. Rev. Ecol. Syst. 19 207–33.

    Google Scholar 

  • Galen, C., Shore, J.S. and Deyoe, H. (1991) Ecotypic divergence in alpinePolemonium viscosum: genetic structure, quantitative variation, and local adaptation.Evolution 45 1218–28.

    Google Scholar 

  • Grant, P.R. (1972) Convergent and divergent character displacement.Biol. J. Linn. Soc. 4 39–68.

    Google Scholar 

  • Grant, P.R. (1975) The classical case of character displacement.Evol. Biol. 8 237–337.

    Google Scholar 

  • Gross, M.R. (1985) Disruptive selection for alternative life histories in salmon.Nature 313 47–8.

    Google Scholar 

  • Gross, M.R. and Charnov, E.L. (1980) Alternative male life histories in bluegill sunfish.Proc. Natl. Acad. Sci USA 77 6937–40.

    Google Scholar 

  • Grudzien, T.A. and Turner, B.J. (1984) Direct evidence that the Ilyodon morphs are a single biological species.Evolution 38 402–7.

    Google Scholar 

  • Hindar, K., Ryman, N. and Stahl, G. (1986) Genetic differentiation among local populations and morphotypes of Arctic charr,Salvelinus alpinus.Biol. J. Linn. Soc. 27 269–85.

    Google Scholar 

  • Hori, M. (1993) Frequency-dependent natural selection in the handedness of scale-eating Cichlid fish.Science 260 216–9.

    Google Scholar 

  • James, F.C. (1983) Environmental component of morphological differentiation in birds.Science 221 184–6.

    Google Scholar 

  • Jehl, J.R., Jr, Francine, J. and Bond, S.I. (1990) Growth patterns of two races of California gull raised in a common environment.Condor 92 732–8.

    Google Scholar 

  • Jones, J.S., Leith, B.H. and Rawlings, P. (1977) Polymorphism in cepae: a problem with too many solutions?Ann. Rev. Ecol. Systm. 8 109–43.

    Google Scholar 

  • Joshi, A. and Thompson, J.N. (1995) Trade-offs and the evolution of host specialization.Evol. Ecol. 9 82–92.

    Google Scholar 

  • Kornfield, I., Smith, D.C., Gagnon, P.S. and Taylor, J.N. (1982) The cichlid fish of Cuatro Cienegas, Mexico: direct evidence of conspecificity among distinct trophic morphs.Evolution 36 658–64.

    Google Scholar 

  • Lack, D. (1947)Darwin's Finches. Cambridge University Press, Cambridge.

    Google Scholar 

  • Lauder, G.V. (1989) Caudal fin locomotion in ray-finned fishes: historical and functional analyses.Am. Zool. 29 85–102.

    Google Scholar 

  • Lavin, P.A. and McPhail, J.D. (1987) Morphological divergence and the organization of trophic characters among lacustrine populations of the threespine stickleback (Gasterosteus aculeatus).Can. J. Fish. Aquat. Sci. 44 1820–9.

    Google Scholar 

  • Lawlor, L.R. and Maynard Smith, J. (1976) The coevolution and stability of competing species.Am. Nat. 110 79–99.

    Google Scholar 

  • Levin, D.A. (1988) Local differentiation and the breeding structure of plant populations. InPlant Evolutionary Biology (L.D. Gottlieb and S. Jain, eds), pp. 305–330. Chapman & Hall, London.

    Google Scholar 

  • Liem, K.F. (1974) Evolutionary strategies and morphological innovations: cichlid paryngeal jaws.Syst. Zool. 20 425–41.

    Google Scholar 

  • Lindsey, C.C. (1981) Stocks are chameleons: plasticity in gill rakers of Coregonid fishes.Can. J. Fish. Aquat. Sci. 38 1497–506.

    Google Scholar 

  • Lodi, E. and Malacarne, G. (1991) Differences in sexual behaviour between two phenotypic states of the spined loach,Cobitis taenia L.J. Fish Biol. 38 321–3.

    Google Scholar 

  • MacArthur, R.H. and Levins, R. (1964) Competition, habitat selection and character displacement in a patchy environment.Proc. Natl Acad. Sci. USA 51 1207–10.

    PubMed  Google Scholar 

  • MacArthur, R.H. and Levins, R. (1967) The limiting similarity, convergence and divergence of coexisting species.Am. Nat. 101 377–85.

    Google Scholar 

  • McPhail, J.D. (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia.Can. J. Zool. 62 1402–8.

    Google Scholar 

  • McPhail, J.D. (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species pair in Paxton Lake, Texada Island, British Columbia.Can. J. Zool. 70 361–9.

    Google Scholar 

  • Magnuson, J.J. and Heitz, J.G. (1971) Gill raker apparatus and food selectivity among mackerels, tunas, and dolphins.Fish. Bull. 69 361–70.

    Google Scholar 

  • Magnusson, K.P. and Ferguson, M.M. (1987) Genetic analysis of four sympatric morphs of Arctic charr,Salvelinus alpinus, from Thigvallavatn, Iceland.Environ. Biol. Fish. 20 67–73.

    Google Scholar 

  • Magurran, A.E. (1990) The inheritance and development of minnow anti-predator behavior.Anim. Behav. 39 828–34.

    Google Scholar 

  • Malmquist, H.J. (1992) Phenotype-specific feeding behavior of two Arctic charrSalvelinus alpinus morphs.Oecologia 92 354–61.

    Google Scholar 

  • Maynard Smith, J. (1982)Evolution and the Theory of Games. Cambridge University Press, Cambridge.

    Google Scholar 

  • Maynard Smith, J. (1987) When learning guides evolution.Nature 329 761–2.

    PubMed  Google Scholar 

  • Mayr, E. (1963)Animal Species and Evolution. Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Meacham, C.A. and Duncan, T. (1989)MorphoSys 1.24. University Herbarium, University of California at Berkely, Berkely, CA.

    Google Scholar 

  • Meyer, A. (1987) Phenotypic plasticity and heterochrony inCichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes.Evolution 41 1357–69.

    Google Scholar 

  • Meyer, A. (1989) Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fish,Cichlasoma citrinellum.Oecologia 80 431–436.

    Google Scholar 

  • Meyer, A. (1990) Ecological and evolutionary consequences of the trophic polymorphism inCichlasoma citrinellum (Pisces, Cichlidae).Biol. J. Linn. Soc. 39 279–99.

    Google Scholar 

  • Mittelbach, G.G., Osenberg, C.W. and Wainwright, P.C. (1992) Variation in resource abundance affects diet and feeding morphology in the pumpkinseed sunfish (Lepomis gibbosus).Oecologia 90 8–13.

    Google Scholar 

  • Moore, J.A. (1952) Competition betweenDrosophila melanogaster andDrosophila simulans. II. The improvement of competitive ability through selection.Proc. Natl Acad. Sci. USA 38 813–17.

    Google Scholar 

  • Owen, D.F. and Whiteley, D. (1989) Evidence that reflexive polymorphisms are maintained by visual selection by predators.Oikos 55 130–3.

    Google Scholar 

  • Patton, J.L. and Brylski, P.V. (1987) Pocket gophers in alfalfa fields: causes and consequences of habitatrelated body size variation.Am. Nat. 130 493–506.

    Google Scholar 

  • Pedhazur, E.H. (1982)Multiple Regression in Behavioral Research, Explanation and Prediction, 2nd edn. Holt, Rinehart and Winston, New York.

    Google Scholar 

  • Pimm, S.L. (1978) Sympatric speciation: a simulation model.Biol. J. Linn. Soc. 11 131–9.

    Google Scholar 

  • Robinson, B.W. (1994)Evolutionary ecology of phenotypic polymorphisms in fishes. PhD dissertation, Binghamton University, Binghamton, NY.

    Google Scholar 

  • Robinson, B.W. and Wilson, D.S. (1994) Character release and displacement in fishes: a neglected literature.Am. Nat. 144 596–627.

    Google Scholar 

  • Robinson, B.W. and Wilson, D.S. (1995) Experimentally induced morphological diversity in Trinidadian guppies (Poecilia reticulata).Copeia 1995, 294–305.

    Google Scholar 

  • Robinson, B.W., Wilson, D.S., Margosian, A.S. and Lotito, P.T. (1993) Ecological and morphological differentiation by pumpkinseed sunfish in lakes without bluegill sunfish.Evol. Ecol. 7 451–64.

    Google Scholar 

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

    Google Scholar 

  • Robinson, B.W., Wilson, D.S. and Margosian, A.S. (undated). The effect of a closely related competitor, other fish species and the physical environment on the pumpkinseed (Lepomis gibbosus) trophic polymorphism. Unpublished manuscript.

  • Rosenzweig, M.L. (1978) Competitive speciation.Biol. J. Linn. Soc. 10 274–89.

    Google Scholar 

  • Rosenzweig, M.L. (1981) A theory of habitat selection.Ecology 62 327–35.

    Google Scholar 

  • Rosenzweig, M.L. (1991) Habitat selection and population interactions: the search for mechanism.Am. Nat. 137 s5–28.

    Google Scholar 

  • Ryan, M.J. and Causey, B.A. (1989) ‘Alternative’ mating behavior in the swordtailsXiphophorous nigrensis andXiphophorus pygmaeus (Pisces: Poeciliidae).Behav. Ecol. Sociobiol. 24 341–8.

    Google Scholar 

  • Ryman, N., Allendorf, F.W. and Stahl, G. (1979) Reproductive isolation with little genetic divergence in sympatric populations of Brown trout (Salmo trutta).Genetics 92 247–62.

    PubMed  Google Scholar 

  • Sage, R.D. and Selander, R.K. (1975) Trophic radiation through polymorphism in cichlid fishes.Proc. Natl Acad. Sci. USA 72 4669–73.

    Google Scholar 

  • Sandlund, O.T., Jonsson, B., Malmquist, H.J., Gydemo, R., Lindem, T., Skulason, S., Snorrason, S.S. and Jonasson, P.M. (1987) Habitat use of Arctic charrSalvelinus alpinus in Thingvallavatn, Iceland.Environ. Biol. Fish. 20 263–74.

    Google Scholar 

  • Schlichting, C.D. (1989) Phenotypic integration and environmental change.BioScience 39 460–4.

    Google Scholar 

  • Schluter, D. (1994) Experimental evidence that competition promotes divergence in adaptive radiation.Science 266 798–801.

    Google Scholar 

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

    Google Scholar 

  • Schluter, D. and McPhail, J.D. (1992) Ecological character displacement and speciation in sticklebacks.Am. Nat. 140 85–108.

    Google Scholar 

  • Schluter, D. and McPhail, J.D. (1993) Character displacement and replicate adaptive radiation.Trends Ecol. Evol. 8 197–200.

    Google Scholar 

  • Shuster, S.M. (1989) Male alternative reproductive strategies in a marine isopod crustacean (Paracerceis sculpta): the use of genetic markers to measure differences in fertilization success among alpha, beta and gamma males.Evolution 43 1683–98.

    Google Scholar 

  • Skulason, S. and Smith, T.B. (1995) Resource polymorphisms in vertebrates.TREE 10, 366–70.

    Google Scholar 

  • Skulason, S., Antonsson, T., Gudbergsson, G., Malmquist, H.J. and Snorrason, S.S. (1992) Variability in Icelandic Arctic charr.Icel. Agr. Sci. 6 143–53.

    Google Scholar 

  • Skulason, S., Snorrason, S.S., Ota, D. and Noakes, D.L.G. (1993) Genetically based differences in foraging behaviour among sympatric morphs of arctic charr (Pisces: Salmonidae).Anim. Behav. 45 1179–92.

    Google Scholar 

  • Smith, T.B. (1987) Bill size polymorphism and intraspecific niche utilization in an African finch.Nature 329 717–19.

    Google Scholar 

  • Smith, T.B. (1990a) Natural selection on bill characters in the two bill morphs of the African finchPyrenestes ostrinus.Evolution 44 832–42.

    Google Scholar 

  • Smith, T.B. (1990b) Resource use by bill morphs of an African finch: evidence for intraspecific competition.Ecology 71 1246–57.

    Google Scholar 

  • Smith, T.B. and Temple, S.A. (1982) Feeding habits and bill polymorphism in Hook-billed Kites.Auk 99 197–207.

    Google Scholar 

  • Snorrason, S.S., Skulason, S., Jonsson, B., Malmquist, H.J., Jonasson, P.M., Sandlund, O.T. and Lindem, T. (1994a) Trophic specialization in Arctic charrSalvelinus alpinus (Pisces: Salmonidae): morphological divergence and ontogenetic niche shifts.Biol. J. Linn. Soc. 52 1–18.

    Google Scholar 

  • Snorrason, S.S., Skulason, S., Sandlund, O.T., Malmquist, H.J., Jonsson, B. and Jonasson, P.M. (1994b) Shape polymorphism in sympatric arctic charr,Salvelinus alpinus, in Thingvallavatn, Iceland. InBiology of Charrs and Masu Salmon (H. Kawanabe, F. Yamazaki and D.L.G. Noakes, eds), pp. 393–404. Kyoto University Press, Kyoto.

    Google Scholar 

  • Sokal, R.R. and Rohlf, F.J. (1981)Biometry. W.H. Freeman and Co, New York.

    Google Scholar 

  • Stearns, S.C. (1989) The evolutionary significance of phenotypic plasticity.BioScience 39 436–45.

    Google Scholar 

  • Stephens, D.W. and Krebs, J.R. (1986)Foraging Theory. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Todd, T.N., Smith, G.R. and Cable, L. (1981) Environmental and genetic contributions to morphological differentiation in ciscoes (Coregoninae) of the Great Lakes.Can. J. Fish. Aquat. Sci. 38 59–67.

    Google Scholar 

  • Trexler, J.C., Travis, J. and Trexler, M. (1990) Phenotypic plasticity in the Sailfin Molly,Poecilia latipinna (Pisces: Poeciliidae). II. Laboratory experiment.Evolution 44 157–67.

    Google Scholar 

  • Turner, B.J., Grudzien, T.A., Adkisson, K.P. and White, M.M. (1983) Evolutionary genetics of trophic differentiation in goodeid fishes of the geneus Ilyodon.Environ Biol. Fish. 9 159–72.

    Google Scholar 

  • van den Berghe, E.P., Wernerus, F. and Warne, R.R. (1989) Female choice and mating cost of peripheral males.Anim. Behav. 38 875–84.

    Google Scholar 

  • Via, S. and Lande, R. (1985) Genotype—environment interaction and the evolution of phenotypic plasticity.Evolution 39 505–22.

    Google Scholar 

  • Videler, J.J. (1993)Fish Swimming. Chapman & Hall, London.

    Google Scholar 

  • Wainwright, P.C., Osenberg, S.W. and Mittelbach, G.G. (1991) Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): effects of environment on ontogeny.Funct. Ecol. 5 40–55.

    Google Scholar 

  • Webb, P.W. (1975) Hydrodynamics and energetics of fish propulsion.Bull. Fish. Res. Bd Can. 190 1–158.

    Google Scholar 

  • Webb, P.W. (1984a) Body form, locomotion and foraging in aquatic vertebrates.Am. Zool. 24 107–20.

    Google Scholar 

  • Webb, P.W. (1984b) Form and function in fish swimming.Sci. Am. 251 72–82.

    Google Scholar 

  • Weihs, D. (1989) Design features and mechanics of axial locomotion in fish.Am. Zool. 29 151–60.

    Google Scholar 

  • West-Eberhard, M.J. (1989) Phenotypic plasticity and the origins of diversity.Ann. Rev. Ecol. Syst. 20 249–78.

    Google Scholar 

  • Wilkinson, L. (1989)Systat: The System for Statistics. Systat Inc., Evanson, IL.

    Google Scholar 

  • Wilson, D.S. (1989) The diversification of single gene pools by density- and frequency-dependent selection. InSpeciation and its Consequences (D. Otte and J.A. Endler, eds), pp. 366–85. Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Wilson, D.S. and Turelli, M. (1986) Stable underdominance and the evolutionary invasion of empty niches.Am. Nat. 127 835–50.

    Google Scholar 

  • Wilson, D.S. and Yoshimura, J. (1994) On the coexistence of specialists and generalists.Am. Nat. 144 692–707.

    Google Scholar 

  • Wimberger, P. (1991) Plasticity of jaw and skull morphology in the neotropical cichlidsGeophagus brasiliensis andG. steindachneri.Evolution 45 1545–63.

    Google Scholar 

  • Wimberger, P. (1992) Plasticity of fish body shape: the effects of diet, development, family and age in two species ofGeophagus (Pisces: Cichlidae).Biol. J. Linn. Soc. 45 197–218.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Binghamton University, 13902-6000, Binghamton, NY, USA

    Beren W. Robinson & David Sloan Wilson

Authors
  1. Beren W. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Sloan Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Robinson, B.W., Wilson, D.S. Genetic variation and phenotypic plasticity in a trophically polymorphic population of pumpkinseed sunfish (Lepomis gibbosus). Evol Ecol 10, 631–652 (1996). https://doi.org/10.1007/BF01237711

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01237711

Keywords

Search

Navigation