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Mapping Phenotypes: Canalization, Plasticity and Developmental Stability

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Mapping Phenotypes: Canalization, Plasticity and Developmental Stability Opinion TRENDS in Ecology & Evolution Vol.16 No.10 October 2001 555 Canalization Mapping phenotypes: Canalization was first defined by Waddington11,12 as the ability to produce a consistent phenotype in spite of variable genetic and/or environmental features canalization, plasticity (Box 1). Later13,14, Waddington broadened this definition, focusing on phenotypes that, if not strictly invariable, are ‘to some extent resistant to and developmental modification’. Simultaneously, he developed the idea of canalizing selection, implying a genetic control of canalization. Waddington thought that the same stability process counteracted both genetic and environmental disturbances. This duality is the basis of ‘genetic assimilation’, the process by which a response to Vincent Debat and Patrice David unusual environments can be converted by selection into a permanent, genetically determined, phenotypic change. In parallel, Schmalhausen15 developed the The relationship between genotype and phenotype is not one to one. This related concept of the ‘auto-regulatory mechanism’ statement is central to our understanding of how natural selection shapes (Box 1), a process that stabilizes the morphology phenotypic evolution. Here, we clarify the links between canalization, plasticity against environmental influences and mutations. He and developmental stability, the three major processes involved in the control also recognized that some labile organisms showed of phenotypic variability. We present a short historical review, including the environmentally induced changes in development, original definitions of these concepts, and then summarize their current although he never used the term ‘plasticity’. meaning and use, highlighting possible sources of confusion. Some of the Thoday16, in defining ‘developmental flexibility’, perspectives allowed by a more synthetic conceptual framework are presented, explicitly introduced an adaptive value to the in the light of the recent advances in molecular and developmental genetics. processes involved in developmental control (Box 1). One of the most important advances achieved through Phenotypic plasticity the evolutionary synthesis is the consideration of Woltereck17 introduced the concept of the ‘reaction phenotypic variation as a quantity of interest, whereas, norm’ as early as 1909, but Johannsen was the first to according to the classic typological view, it is considered point out the general importance of environmental a nuisance. Thus, the factors affecting phenotypic influences for genotype–phenotype relationships18. variation have been given considerable attention by Schmalhausen (Box 1) used two different terms to evolutionists. It is widely accepted that variability describe such influences, depending on their adaptive (defined as the ability to vary1–3) results from two or nonadaptive nature15. The definition of plasticity antagonistic trends4: on the one hand, sources of given by Bradshaw19 encompasses both variation, including genetic mutations, environmental Schmalhausen’s concepts (Box 1). Smith-Gill20 effects and developmental errors; on the other hand, a recently distinguished two different components in set of regulatory processes, including buffering and plasticity, focusing on the discrete versus continuous enhancing mechanisms. Three such processes are variation of the traits in relation to their adaptive commonly considered: canalization, phenotypic value (Box 1). plasticity and developmental stability. Much effort has been made recently to understand the genetic Developmental stability bases, evolvability and evolutionary implications of Physiological homeostasis ensures a constant end these processes5–8. However, the literature can be product in spite of disturbances10. Lerner’s21 confusing, because the historical definitions usually extension of this concept (‘genetic homeostasis’, Vincent Debat* referred to do not take into account later conceptual Box 1) is the basis of many later studies dealing with Laboratoire Génétique et and empirical advances. Most modern authors correlations between heterozygosity and Environnement, Institut consider each of the three processes separately, morphological variance22,23. In this context, des Sciences de 5 l’Evolution, UMR 5554 although their distinction might appear arbitrary . individual deviations from the population mean CNRS, CC064, Université were often interpreted as developmental errors, Montpellier II, 34095 Historical context: the origin of disorder revealing a lack of developmental stability or Montpellier Cedex 05, The study of developmental regulatory processes is developmental homeostasis, taken as synonyms of France. *e-mail: rooted in the old concept of physiological homeostasis, Waddington’s canalization. However, the use of the [email protected] defined by Bernard9 and Cannon10. word ‘homeostasis’ at both the individual and montp2.fr Developmentalists, such as Waddington and population levels is confusing and was rejected by 13 Patrice David Schmalhausen, suggested that developmental Waddington , and many researchers argued that Centre d’Ecologie pathways, as well as physiology, must be strongly these concepts were unnecessary to explain the Fonctionnelle et Evolutive controlled. The concepts of canalization, plasticity observed correlations24. In addition to (CEFE) CNRS, route de Mende, 34095 Montpellier and stability were developed to describe such morphological variance, the deviation from Cedex 05, France. control systems. bilateral symmetry, or ‘fluctuating asymmetry’(FA), http://tree.trends.com 0169-5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02266-2 556 Opinion TRENDS in Ecology & Evolution Vol.16 No.10 October 2001 Box 1. Canalization, plasticity and developmental stability: some historical landmarks in the evolution of three concepts We provide original definitions whenever • Bradshaw, 1965e: phenotypic plasticity: • Bradshaw, 1965e: developmental they are short and self-explanatory. ‘Plasticity is shown by a genotype when instability is plasticity. According to Otherwise we provide a concise summary its expression is able to be altered by Bradshaw, stochastic errors during of the author’s ideas. environmental influences…it does not development (referred to as have any implication concerning the ‘developmental instability’) must be Canalization adaptive value of the change occurring, viewed as a manifestation of plasticity, • Waddington, 1942a: canalization: although many types of plasticity may considering that ‘such changes ‘Adjustment of developmental reactions have important adaptive effects’. ultimately have definite environmental so as to bring about one definite end result • Smith-Gill, 1983f: plasticity, developmental causes’. regardless of minor variations in conversion and phenotypic modulation. • Zakharov, 1992h: developmental conditions during the course of the Plasticity is separated by Smith-Gill into homeostasis, homeorhesis, reaction’. two different components: developmental stability. Zakharov • Waddington, 1961b: canalization: ‘The ‘developmental conversion’ is an redefined developmental homeostasis property of a developmental process, of adaptive discrete change; whereas (or ‘homeorhesis’) as the set of being to some extent modifiable, but to ‘phenotypic modulation’ is a continuous mechanisms ensuring phenotypic some extent resistant to modification’. nonadaptive variation. Only the former consistency, including two different and • Schmalhausen, 1949c: autoregulatory is supposed to be genetically based and well-separated processes: canalization, mechanism: ‘a set of processes historically therefore moulded by selection. corresponding to Schmalhausen’s selected, monitoring developmental path’. Additionally, she proposed modulation ‘autonomous-regulatory development’; • Thoday, 1953d: developmental flexibility: to result from ‘a failure of the organism to and developmental stability, a set of ‘an individual organism may be said to completely buffer development against mechanisms buffering developmental possess flexibility either if its genotype is environmental perturbations’, or explicitly noise sensu Waddington, that is, such that it can develop different formulated, as a lack of canalization. developmental variation among phenotypes in different environments, replicated or symmetrical organs within each phenotype better adapted than the Developmental stability a single organism. others to the environment that evokes it, • Lerner, 1954g: genetic homeostasis, or if its genotype is so balanced that developmental homeostasis, References development is buffered against developmental stability. Lerner defined a Waddington, C.H. (1942) Canalization of environmental variables and hence genetic homeostasis as ‘the property of development and the inheritance of acquired characters. Nature 150, 563–565 apparently the same adaptive the population to equilibrate its genetic b Waddington, C.H. (1961) Genetic assimilation. phenotype results in a range of composition and to resist to sudden Adv. Genet. 10, 257–293 environmental conditions’. changes’. According to him, this property c Schmalhausen, I.I. (1949) Factors of Evolution, depends on population heterozygosity, University of Chicago Press Plasticity as heterozygous individuals buffer d Thoday, J.M. (1953) Components of fitness. • Schmalhausen, 1949c: morphosis and developmental variation more efficiently Symp. Soc. Exp. Biol. 7, 97–113 e Bradshaw, A.D. (1965) Evolutionary dependent autoregulatory
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