Phenotypic flexibility and the evolution of organismal design

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Abstract

Evolutionary biologists often use phenotypic differences between species and between individuals to gain an understanding of organismal design. The focus of much recent attention has been on developmental plasticity – the environmentally induced variability during development within a single genotype. The phenotypic variation expressed by single reproductively mature organisms throughout their life, traditionally the subject of many physiological studies, has remained underexploited in evolutionary biology. Phenotypic flexibility, the reversible within-individual variation, is a function of environmental conditions varying predictably (e.g. with season), or of more stochastic fluctuations in the environment. Here, we provide a common framework to bring the different categories of phenotypic plasticity together, and emphasize perspectives on adaptation that reversible types of plasticity might provide. We argue that better recognition and use of the various levels of phenotypic variation will increase the scope for phenotypic experimentation, comparison and integration.

Section snippets

Phenotypic flexibility

When environmental conditions change rapidly and over shorter timescales than a lifetime, individuals that can show continuous but reversible transformations in behaviour, physiology and morphology might incur a selective advantage 18, 22, 25. There are now several studies documenting substantial but reversible phenotypic changes within adult organisms, especially with regard to the sizes of organ systems in relation to metabolic demand 23, 26, 27.

The most dramatic examples of reversible

Cyclic phenotypic variation: the life-cycle stage concept

In seasonal environments, different activities related to reproduction and survival (breeding, moult, migration, hibernation, etc.) are usually separated in time within individuals, and tend to occur at predictable times of the year, accompanied by changes in the mature adult phenotype [44]. To perform optimally under a wide range of environmental conditions (variations that are often cyclic) by tracking or anticipating the external changes, a long-lived individual must regulate gene expression

The nature of plasticity in environments differing in predictability

The accuracy with which future environmental conditions can be predicted could determine the kind of phenotypic plasticity that one might expect to evolve 25, 48, 49. In unpredictable environments, a capacity for rapid and reversible phenotypic change (flexibility) will have obvious fitness payoffs [25]. Where environmental conditions vary in a temporarily predictable way, long-lived organisms can anticipate the changes by showing sequences of life-cycle stages 39, 45. The seasonal template for

Interpreting phenotypic flexibility: a study of adaptation?

In evolutionary biology, a phenotypic trait can be considered to be an adaptation only if there is evidence that it has been moulded in specific ways during its evolutionary history to make it more effective for its particular role [56]. Together with Feder and Watt 57, 58, we believe that the functional study of phenotype–environment interactions is necessary for evolutionary insight; that is, an ‘amechanistic’ worldview is no longer satisfactory [58]. Rather than emphasizing that a capacity

Conclusions

Our discussion complements three recent books about phenotypic plasticity 3, 8, 11 and two reviews of evolutionary and ecological physiology 66, 67. It enlarges the scope of their viewpoints to bring the various kinds of phenotypic variation together within a common framework and it emphasizes the potential of intra-individual phenotypic variation for biological discovery (see [68] for a discussion that includes variation between genotypes). The extent to which individuals can respond to

Acknowledgements

Our research was supported by a PIONIER-grant from The Netherlands Organization for Scientific Research (NWO) to T.P. and a NOP-grant to J.D. We thank Bob Ricklefs, John Wingfield, Martin Wikelski, Doug Levey, Pieternella Luttikhuizen, Maurine Dietz, Wouter Vahl, Jeroen Reneerkens, Pim Edelaar, Isabel Smallegange, Jaap van der Meer, Irene Tieleman, Ward B. Watt, Joe B. Williams and two anonymous referees for discussion, editorial help and other input. Dick Visser drew the figures.

References (74)

  • J. Travis

    Evaluating the adaptive role of morphological plasticity

  • S.E. Sultan

    Phenotypic plasticity and plant adaptation

    Acta Bot. Neerl.

    (1995)
  • D. Reznick et al.

    The empirical study of adaptation in natural populations

  • C.D. Schlichting et al.

    Phenotypic Evolution: A Reaction Norm Perspective

    (1998)
  • J. Travis

    Sources of variation in physiological phenotypes and their evolutionary significance

    Am. Zool.

    (1999)
  • L.J. Chapman

    Phenotypic plasticity and the possible role of genetic assimilation: hypoxia-induced trade-offs in the morphological traits of an African cichlid

    Ecol. Lett.

    (2000)
  • M. Pigliucci

    Phenotypic Plasticity

    (2001)
  • S. Stearns

    The evolutionary significance of phenotypic plasticity

    Bioscience

    (1989)
  • A.M. Shapiro

    Seasonal polyphenism

    Evol. Biol.

    (1976)
  • H.V. Danks

    Life cycles in polar arthropods – flexible or programmed?

    Eur. J. Entomol.

    (1999)
  • P.E. Komers

    Behavioural plasticity in variable environments

    Can. J. Zool.

    (1997)
  • C.K. Ghalambor et al.

    Comparative manipulation of predation risk in incubating birds reveals variability in the plasticity of responses

    Behav. Ecol.

    (2002)
  • C.L. Prosser

    Environmental and Metabolic Animal Physiology: Comparative Animal Physiology

    (1991)
  • P. Willmer

    Environmental Physiology of Animals

    (2000)
  • A.H. Woods et al.

    Interpreting rejections of the beneficial acclimation hypothesis: when is physiological plasticity adaptive?

    Evolution

    (2002)
  • S.M. Scheiner

    Genetics and evolution of phenotypic plasticity

    Annu. Rev. Ecol. Syst.

    (1993)
  • J.G. Kingsolver et al.

    Evolutionary analyses of morphological and physiological plasticity in thermally variable environments

    Am. Zool.

    (1998)
  • J.M. Starck

    Structural flexibility of the gastro-intestinal tract of vertebrates – implications for evolutionary morphology

    Zool. Anz.

    (1999)
  • D.K. Padilla et al.

    Plastic inducible morphologies are not always adaptive: the importance of time delays in a stochastic environment

    Evol. Ecol.

    (1996)
  • K.A. Hammond

    Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient

    J. Exp. Biol.

    (2001)
  • J.M. Starck et al.

    Structural flexibility of the intestine of Burmese python in response to feeding

    J. Exp. Biol.

    (2001)
  • D.R. Levitan

    Density-dependent size regulation in Diadema antillarum: effects on fecundity and survivorship

    Ecology

    (1989)
  • D.R. Levitan

    Skeletal changes in the test and jaws of the sea urchin Diadema antillarum in response to food limitation

    Mar. Biol.

    (1991)
  • B. Marinovic et al.

    Krill can shrink as an ecological adaptation to temporarily unfavourable environments

    Ecol. Lett.

    (1999)
  • S.M. Secor

    Rapid upregulation of snake intestine in response to feeding: a new model of intestinal adaptation

    Am. J. Physiol.

    (1994)
  • S.M. Secor et al.

    A vertebrate model of extreme physiological regulation

    Nature

    (1998)
  • T. Madsen et al.

    Do snakes shrink?

    Oikos

    (2001)
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