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Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail

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Abstract

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.

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References

  • Ament, A.S., 1979. Geographic variation in relation to life history in three species of the marine gastropod genus Crepidula: growth rates of newly hatched larvae and juveniles, pp. 61–76 in Reproductive Ecology of Marine Invertebrates, edited by S.E. Stancyk. University. of South Carolina Press, Columbia, S.C.

    Google Scholar 

  • Appleton, R.D. & A.R. Palmer, 1988. Water-borne stimuli released by crabs and damaged prey induce more predator-resistant shells in a marine gastropod. Proc. Natl. Acad. Sci. USA 85: 4387–4391.

    Google Scholar 

  • Baldwin, I.T. & J.C. Schultz, 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221: 277–279.

    Google Scholar 

  • Bertness, M.D., 1999. The Ecology of Atlantic Shorelines. Sinauer, Sunderland, M.A.

    Google Scholar 

  • Bertness, M.D. & C. Cunningham, 1981. Crab shell-crushing predation and gastropod architectural defense. J. Exp. Mar. Biol. Ecol. 50: 213–230.

    Google Scholar 

  • Berven, K.A. & D.E. Gill & S.J. Smith-Gill, 1979. Countergradient selection in the green frog, Rana clamitans. Evolution 33: 609–623.

    Google Scholar 

  • Boucot, A.J., 1982. Ecophenotypic or genotypic? Nature 296: 609–610.

    Google Scholar 

  • Boulding, E.G., 1990. Are the opposing selection pressures on exposed and protected shores sufficient to maintain genetic differentiation between gastropod populations with high intermigration rates? Hydobiologia 193: 41–52.

    Google Scholar 

  • Boulding, E.G. & K.L. VanAlstyne, 1993. Mechanisms of differential survival and growth of two species of Littorina on wave-exposed and protected shores. J. Exp. Mar. Biol. Ecol. 169: 139–166.

    Google Scholar 

  • Bradshaw, A.D., 1965. Evolutionary significance of phenotypic plasticity. Adv. Genet. 13: 115–155.

    Google Scholar 

  • Carter, J.G., 1980. Environmental and biological controls of bivalve shell mineralogy and microstructure, pp. 69–113 in Skeletal Growth in Aquatic Organisms, edited by D.C. Rhoads & R.A. Lutz. Plenum Press, New York.

    Google Scholar 

  • Chamberlin, J.A. & R.R. Graus, 1975. Water flow and hydromechanical adaptations of branched reef corals. Bull. Mar. Sci. 25: 112–125.

    Google Scholar 

  • Charlesworth, B. & R. Lande, 1982. Morphological stasis and developmental constraint: no problem for neo-Darwinism. Nature 296: 610.

    Google Scholar 

  • Conover, D.O. & E.T. Schultz, 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol. Evol. 10: 248–252.

    Google Scholar 

  • Conover, D.O. & T.M.C. Present, 1990. Countergradient variation in growth rate: compensation for length of growing season among Atlantic silversides from different latitudes. Oecologia (Berl.) 83: 316–324.

    Google Scholar 

  • Craig, J.K. & C.J. Foote, 2001. Countergradient variation and secondary sexual color: phenotypic convergence promotes genetic divergence in carotenoid use between sympatric anadromous and nonanadramous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 55: 380–391.

    Google Scholar 

  • Crothers, J.H., 1983. Some observations on shell-shape variation in North American populations of Nucella lapillus (L.). Biol. J. Linn. Soc. 19: 237–274

    Google Scholar 

  • Dayton, P.K., 1971. Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41: 351–389.

    Google Scholar 

  • Dehnel, P., 1955. Rates of growth of gastropods as a function of latitude. Phys. Zool. 28: 115–144.

    Google Scholar 

  • Denny, M.W., 1988. Biology and the Mechanics of theWave-Swept Environment. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Denny, M.W. & T.L. Daniel & M.A.R. Koehl, 1985. Mechanical limits to size in wave-swept organisms. Ecol. Monogr. 55: 69–102.

    Google Scholar 

  • Dewitt, T.J. & A. Sih & D.S. Wilson, 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13: 77–81.

    Google Scholar 

  • Dobzhansky, T., 1951. Genetics and the Origin of Species. Columbia University Press, New York, N.Y.

    Google Scholar 

  • Dodd, J.R., 1963. Paleoecological implications of shell mineralogy in two pelecypod species. J. Geol. 71: 1–11.

    Google Scholar 

  • Dodson, S.I., 1989. Predator-induced reaction norms. Bioscience 39: 447–453.

    Google Scholar 

  • Dudgeon, S.R. & A.S. Johnson, 1992. Thick versus thin: thallus morphology and tissue mechanics influence differential drag and dislodgement of two co-dominant seaweeds. J. Exp. Mar. Biol. Ecol. 165: 23–43.

    Google Scholar 

  • Endler, J.A., 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Etter, R.J., 1988a. Asymmetrical developmental plasticity in an intertidal snail. Evolution 42: 322–334.

    Google Scholar 

  • Etter, R.J., 1988b. Physiological stress and color polymorphism in the intertidal snail Nucella lapillus. Evolution 42: 660–680.

    Google Scholar 

  • Etter, R.J., 1989. Life history variation in the intertidal snail Nucella lapillus across a wave-exposure gradient. Ecology 70: 1857–1876.

    Google Scholar 

  • Gilbert, J.J., 1966. Rotifer ecology and embryological induction. Science 151: 1234–1237.

    Google Scholar 

  • Gillespie, J.H. & M. Turelli, 1989. Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121: 129–138.

    Google Scholar 

  • Gingerich, P.D., 1993. Quantification and comparison of evolutionary rates. Am. J. Sci. 293A: 453–478.

    Google Scholar 

  • Gotthard, K. & S. Nylin, 1995. Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life history. Oikos 74: 3–17.

    Google Scholar 

  • Graus, R.R. & J.A. Chamberlin & A.M. Boker, 1977. Structural modifications of corals in relation to waves and currents. Studs. Geol. 4: 135–153.

    Google Scholar 

  • Graus, R.R., 1974. Latitudinal trends in the shell characteristics of marine gastropods. Lethaia 7: 303–314.

    Google Scholar 

  • Hadlock, R.P., 1980. Alarm responses of the intertidal snail Littorina littorea (L.) to predation by the crab Carcinus maenas (L.). Biol. Bull. 159: 269–279.

    Google Scholar 

  • Hendry, A.P. & M.T. Kinnison, 1999. The pace of modern life: measuring rates of contemporary microevolution. Evolution 53: 1637–1653.

    Google Scholar 

  • James, F.C., 1983. Environmental component of morphological differentiation in birds. Science 221: 184–186.

    Google Scholar 

  • Janson, K., 1983. Multivariate morphometric analysis of two varieties of Littorina saxatilis from the Swedish west coast. Mar. Biol. 74: 49–53.

    Google Scholar 

  • Johannesson, B., 1986. Shell morphology of Littorina saxatilis Olivi: the relative importance of physical factors and predation. J. Exp. Mar. Biol. Ecol. 102: 183–195.

    Google Scholar 

  • Karban, R. & I.T. Baldwin, 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, I.L.

    Google Scholar 

  • Karban, R. & A.A. Agrawal & M. Mangel, 1997. The benefits of induced defenses against herbivores. Ecology 78: 1351–1355.

    Google Scholar 

  • Kemp, P. & M.D. Bertness, 1984. Snail shape and growth rates: evidence for plastic allometry in Littorina littorea. Proc. Natl. Acad. Sci. USA 81: 811–813.

    Google Scholar 

  • Kitching, J.A. & L. Muntz & F.J. Ebling, 1966. The ecology of Lough Ine. XV. The ecological significance of shell and body forms in Nucella. J. Anim. Ecol. 35: 113–126.

    Google Scholar 

  • Leonard, G.H. & M.D. Bertness & P.O. Yund, 1999. Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80: 1–14.

    Google Scholar 

  • Levins, R., 1969. Thermal acclimation and heat resistance in Drosophila species. Am. Nat. 103: 483–499.

    Google Scholar 

  • Lively, C.M., 1986. Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40: 232–242.

    Google Scholar 

  • Losos, J.B. & K.I. Warheit & T.W. Schoener, 1997. Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387: 70–73.

    Google Scholar 

  • Losos, J.B. & D.A. Creer, D. Glossip, R. Goellner, A. Hampton, G. Roberts, N. Haskell, P. Taylor & J. Ettling, 2000. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54: 301–305.

    Google Scholar 

  • Losos, J.B. & K.I. Warheit & T.W. Schoener, 2001. Experimental studies of adaptive differentiation in Bahamian Anolis lizards. Genetica 112-113: 399–415.

    Google Scholar 

  • Lowenstam, H., 1954a. Factors affecting the aragonite:calcite ratio in carbonate-secreting marine invertebrates. J. Geol. 62: 285–322.

    Google Scholar 

  • Lowenstam, H., 1954b. Environmental relations of modification compositions of certain carbonate-secreting marine invertebrates. Proc. Natl. Acad. Sci. USA 40: 39–48.

    Google Scholar 

  • Mayr, E., 1963. Animal Species and Evolution. Harvard Univ. Press, Cambridge, M.A.

    Google Scholar 

  • Mayr, E., 1982. Questions concerning speciation. Nature 296: 609.

    Google Scholar 

  • Palmer, A.R., 1979. Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution 33: 697–713.

    Google Scholar 

  • Palmer, A.R., 1981. Do carbonate skeletons limit the rate of body growth? Nature 292: 150–152.

    Google Scholar 

  • Palmer, A.R., 1983. Growth rate as a measure of food value in thaidid gastropods: assumptions and implications for prey morphology and distribution. J. Exp. Mar. Biol. Ecol. 73: 95–124.

    Google Scholar 

  • Palmer, A.R., 1985. Adaptive value of shell variation in Thais lamellosa: effect of thick shells on vulnerability to and preference by crabs. Veliger 27: 349–356.

    Google Scholar 

  • Palmer, A.R., 1990. Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193: 155–182.

    Google Scholar 

  • Palmer, A.R., 1992. Calcification in marine molluscs: how costly is it? Proc. Natl. Acad. Sci. USA 89: 1379–1382.

    Google Scholar 

  • Palumbi, S.R., 1984. Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science 225: 1478–1480.

    Google Scholar 

  • Palumbi, S.R., 1986. How body plans limit acclimation: responses of a demosponge to wave force. Ecology 67: 208–214.

    Google Scholar 

  • Parsons, K.E., 1997. Contrasting patterns of heritable geographic variation in shell morphology and growth potential in the marine gastropod Bembicium vittatum: evidence from field experiments. Evolution 51: 784–796.

    Google Scholar 

  • Pytkowicz, R.M., 1969. Chemical solution of calcium carbonate. Amer. Zool. 9: 673–679.

    Google Scholar 

  • Reimchen, T.E., 1982. Shell size divergence in Littorina mariae and L. obtusata and predation by crabs. Can. J. Zool. 60: 687–695.

    Google Scholar 

  • Rhoades, D.F., 1979. Evolution of plant chemical defense against herbivores, pp. 3–54 in Herbivores: Their Interaction with Sec ondary Metabolites, edited by G.A. Rosenthal & D.H. Janzen. Academic Press, New York, N.Y.

    Google Scholar 

  • Roff, D.A., 1997. Evolutionary Quantitative Genetics. Chapman and Hall, London, UK.

    Google Scholar 

  • Scattergood, L.W., 1952. The distribution of the green crab, Carcinidaes maenas (L.) in the northwestern Atlantic. Fisheries Circular No. 8, Bull. Depar. Sea and Shore Fisher. Augusta, M.E.

    Google Scholar 

  • Scheiner, S.M., 1993a. Genetics and evolution of phenotypic plasticity. Ann. Rev. Ecol. Syst. 24: 35–68.

    Google Scholar 

  • Scheiner, S.M., 1993b. Plasticity as a selectable trait - reply. Am. Nat. 142: 371–373.

    Google Scholar 

  • Schlichting, C.D., 1986. The evolution of phenotypic plasticity in plants. Ann. Rev. Ecol. Syst. 17: 667–693.

    Google Scholar 

  • Schlichting, C.D., 1989. Phenotypic intergration and environmental change. Bioscience 39: 460–464.

    Google Scholar 

  • Schlichting, C.D. & M. Pigliucci, 1993. Control of phenotypic plasticity via regulatory genes. Am. Nat. 142: 366–370.

    Google Scholar 

  • Schlichting, C.D. & M. Pigliucci. 1998. Phenotypic Evolution: A Reaction Norm Perspective. Sinauer Associates, Sunderland, M.A.

    Google Scholar 

  • Schmalhausen, I.I. 1949. Factors of Evolution. Blakiston, Philadelphia, P.A.

    Google Scholar 

  • Seeley, R.H., 1985. Crab predation, developmental rates, and the evolution of shell form in a marine gastropod (Littorina obtusata). Thesis, Yale University.

  • Seeley, R.H., 1986. Intense natural selection caused a rapid morphological transition in a living marine snail. Proc. Natl. Acad. Sci. USA 83: 6897–6901.

    Google Scholar 

  • Smith, L.D. & A.R. Palmer, 1994. Effects of manipulated diet on size and performance of brachyuran crab claws. Science 264: 710–712.

    Google Scholar 

  • Spight, T.M. & J.M. Emlen, 1976. Clutch sizes of two marine snails with a changing food supply. Ecology 57: 1162–1178.

    Google Scholar 

  • Stearns, S.C., 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436–446.

    Google Scholar 

  • Stearns, S.C., 1992. The Evolution of Life Histories. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Stearns, S. & G. DeJong & B. Newman, 1991. The effects of phenotypic plasticity on genetic correlations. Trends. Ecol. Evol. 6: 122–126.

    Google Scholar 

  • Thompson, J.N., 1998. Rapid evolution as an ecological process. Trends. Ecol. Evol. 13: 329–332.

    Google Scholar 

  • Tollrian, R. & C.D. Harvell, 1999. The evolution of inducible defenses: current ideas, pp. 306–321 in The Ecology and Evolution of Inducible Defenses, edited by R. Tollrian & C.D. Harvell. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Toth, G.B. & H. Pavia, 2000. Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). Proc. Natl. Acad. Sci. USA 97: 14418–14420.

    Google Scholar 

  • Trussell, G.C., 1996. Phenotypic plasticity in an intertidal snail: the role of a common crab predator. Evolution 50: 448–454.

    Google Scholar 

  • Trussell, G.C., 1997a. Phenotypic plasticity in the foot size of an intertidal snail. Ecology 78: 1033–1048.

    Google Scholar 

  • Trussell, G.C., 1997b. Phenotypic selection in an intertidal snail: the effects of a catastrophic storm. Mar. Ecol. Prog. Ser. 151: 73–79.

    Google Scholar 

  • Trussell, G.C., 2000a. Phenotypic plasticity in latitudinally separated populations of Littorina obtusata. Evol. Ecol. Res. 2: 803–822.

    Google Scholar 

  • Trussell, G.C., 2000b. Phentoypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54: 151–166.

    Google Scholar 

  • Trussell, G.C. & M.O. Nicklin. Cue sensitivity, inducible defense, and trade-offs: the influence of contrasting periods of contact between a marine snail and a crab predator. Ecology (in press).

  • Trussell, G.C. & A.S. Johnson, S.G. Rudolph & E.S. Gilfillan, 1993. Habitat and size-specific differences in morphology and tenacity in an intertidal snail. Mar. Ecol. Prog. Ser. 100: 135–144.

    Google Scholar 

  • Trussell, G.C. & L.D. Smith, 2000. Induced defenses in response to an invading crab predator: an explanation of historical and geographic phenotypic change. Proc. Natl. Acad. Sci. USA 97: 2123–2127.

    Google Scholar 

  • Van Tienderen, P.H., 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45: 1317–1331.

    Google Scholar 

  • Vermeij, G.J., 1976. Interoceanic differences in vulnerability of shelled prey to crab predation. Nature 260: 135–136.

    Google Scholar 

  • Vermeij, G.J., 1977. The Mesozoic marine revolution: evidence from snail predators and grazers. Paleobiology 3: 245–258.

    Google Scholar 

  • Vermeij, G.J., 1978. Biogeography and Adaptation: Patterns of Marine Life. Harvard University Press, Cambridge, M.A.

    Google Scholar 

  • Vermeij, G.J., 1982. Phenotypic evolution in a poorly dispersing snail after arrival of a predator. Nature 299: 349–350.

    Google Scholar 

  • Vermeij, G.J., 1987. Evolution and Escalation: An Ecological History of Life. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Vermeij, G.J., 1993. A natural History of Shells. Princeton University Press, Princeton, N.J.

    Google Scholar 

  • Vermeij, G.J. & D.E. Schindel & E. Zisper, 1981. Predation through geological time: evidence from gastropod shell repair. Science 214: 1024–1026.

    Google Scholar 

  • Vermeij, G.J. & J.A. Veil, 1978. A latitudinal pattern in bivalve shell gaping. Malacologia 17: 57–61.

    Google Scholar 

  • Vermeij, G.J. & J.D. Currey, 1980. Geographical variation in the strength of Thaidid snail shells. Biol. Bull. 158: 383–389.

    Google Scholar 

  • Via, S., 1993. Adaptive phenotypic plasticity - target or byproduct of selection in a variable environment. Am. Nat. 142: 352–365.

    Google Scholar 

  • Via, S. & R. Lande, 1985. Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39: 505–523.

    Google Scholar 

  • Via, S. & R. Lande, 1987. Evolution of genetic variability in a spatially heterogeneous environment: effects of genotypeenvironment interaction. Genet. Res. 49: 147–156.

    Google Scholar 

  • Via, S. & R. Gomulkiewicz, G. DeJong, S. M. Scheiner, C. D. Schlichting & P. H. Van Tienderen, 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10: 212–217.

    Google Scholar 

  • Vogel, S., 1981. Life in Moving Fluids: The Physical Biology of Flow. Willard Grant, Boston, M.A.

    Google Scholar 

  • Welch, W.R., 1968. Changes in the abundance of the green crab, Carcinus maenas (L.) in relation to recent water temperature changes. Fish. Bull. 67: 337–345.

    Google Scholar 

  • West, K. & A. Cohen & M. Baron, 1991. Morphology and behavior of crabs and gastropods from Lake Tanganyika, Africa: implications for lucustrine predator-prey coevolution. Evolution 45: 589–607.

    Google Scholar 

  • West, K. & A. Cohen, 1996. Shell microstructure of gastropods from Lake Tanganyika, Africa: adaptation, convergent evolution, and escalation. Evolution 50: 672–681.

    Google Scholar 

  • West-Eberhard, M.J., 1989. Phenotypic plasticity and the origins of diversity. Ann. Rev. Ecol. Syst. 20: 249–278.

    Google Scholar 

  • Wethey, D.S., 1985. Catastrophe extinction and species diversity: a rocky intertidal example. Ecology 66: 445–456.

    Google Scholar 

  • Williamson, P.G., 1981. Palaeontological documentation of speciation in Cenozoic molluscs from Turkana basin. Nature 293: 437–443

    Google Scholar 

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Trussell, G.C., Etter, R.J. Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail. Genetica 112, 321–337 (2001). https://doi.org/10.1023/A:1013364527698

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