Phenotypic Plasticity, Costs of Phenotypes, and Costs of Plasticity : Toward an Integrative View
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Phenotypic Plasticity, Costs of Phenotypes,and Costs of Plasticity
Toward an Integrative View
Hilary S. Callahan,a Heather Maughan,b and Ulrich K. Steinerc
aDepartment of Biological Sciences, Barnard College, Columbia University,New York, New York, USA
bDepartment of Zoology, University of British Columbia,Vancouver, British Columbia, Canada
cDepartment of Biology, Stanford University, Stanford, California, USA
Why are some traits constitutive and others inducible? The term costs often appearsin work addressing this issue but may be ambiguously defined. This review distin-guishes two conceptually distinct types of costs: phenotypic costs and plasticity costs.Phenotypic costs are assessed from patterns of covariation, typically between a focaltrait and a separate trait relevant to fitness. Plasticity costs, separable from phenotypiccosts, are gauged by comparing the fitness of genotypes with equivalent phenotypeswithin two environments but differing in plasticity and fitness. Subtleties associatedwith both types of costs are illustrated by a body of work addressing predator-inducedplasticity. Such subtleties, and potential interplay between the two types of costs, havealso been addressed, often in studies involving genetic model organisms. In some in-stances, investigators have pinpointed the mechanistic basis of plasticity. In this vein,microbialwork is especially illuminating andhas three additional strengths. First, infor-mation about the machinery underlying plasticitysuch as structural and regulatorygenes, sensory proteins, and biochemical pathwayshelps link population-level stud-ies with underlying physiological and genetic mechanisms. Second, microbial studiesinvolve many generations, large populations, and replication. Finally, empirical esti-mation of key parameters (e.g., mutation rates) is tractable. Together, these allow forrigorous investigation of gene interactions, drift, mutation, and selectionall potentialfactors influencing the maintenance or loss of inducible traits along with phenotypicand plasticity costs. Messages emerging from microbial work can guide future effortsto understand the evolution of plastic traits in diverse organisms.
Key words: experimental evolution; selection analysis; phenotypic evolution; tradeoffs;life history theory; environmental heterogeneity
In this age of the genome, phenotypic traitssuch as behavior, morphology, and physiologyremain compelling to many researchers. Ecol-ogists, for example, are interested in connect-ing variation in organismal traits with com-munity and ecosystem patterns and processes(Eviner 2004; Miner et al. 2005). Developmen-
Address for correspondence: Hilary S. Callahan, Department of Bio-logical Sciences, Barnard College, Columbia University, 3009 Broadway,New York, NY 10027. Voice: 212-854-5405. email@example.com
tal and molecular geneticists also examine vari-ation in organismal traits, connecting this vari-ation with underlying genetic mechanisms andbiochemical pathways. Ecological geneticistsand other evolutionary biologists are also inter-ested in connecting phenotypes and associatedgenes, as well as in how both phenotypes andgenotypes are altered by multiple evolutionaryprocessessuch as natural selection, migrationand gene flow, functional tradeoffs among mul-tiple traits, pleiotropy, mutation, and genetic
Ann. N.Y. Acad. Sci. 1133: 4466 (2008). C 2008 New York Academy of Sciences.doi: 10.1196/annals.1438.008 44
Callahan et al.: Phenotypic Plasticity, Costs of Phenotypes, and Costs of Plasticity 45
drift (Pigliucci 2001; Lee 2002; Schlichting &Smith 2002; West-Eberhard 2003; Weinig &Schmitt 2004; Pigliucci et al. 2006; Ghalamboret al. 2007; Masel et al. 2007).
To examine the interplay among phenotypictraits, genes, and such processes, a primary taskfor most phenotypic research is simply to exam-ine the scope and pattern of trait variation. Thiscritical task is often complicated by the phe-nomenon of phenotypic plasticity: variation inenvironmental conditions eliciting variation inthe traits expressed by a given genotype. Con-ceptually, studying the phenotypic plasticity oftraits requires recognizing an organism as aduality, as both a phenotype and a genotype.Doing so often involves the concept of a reac-tion norm: a genotypes range of phenotypesexpressed as a function of the environment(Sarkar 1999; Pigliucci 2001). Operationally,studying plastic traits and reaction norms re-quires a biologist to meet a series of challenges.First, one must identify and specify groupsof individuals with similar genotypesclones,half-sibs, artificial selection lines, conspecifics.Then, one must characterize the phenotypes ofthese replicate genotypes when grown in twoor more environments. Next, one must decidewhether to focus not only on the different traitsexpressed in those environments but perhapsalso on the traits plasticities. That is, plasticitycan be conceptualized as a complex trait in andof itself. Finally, one must decide whether oneneeds to obtain information about underlyingphysiological and genetic mechanisms regulat-ing traits and their plasticity (Schlichting 1986;Via et al. 1995; Pigliucci 1996).
Woltereck, studying genetically homoge-neous lines of the small crustacean Daphniaduring the early 20th century, was among thefirst to grapple with the challenge of genotypephenotype mapping. He documented the ef-fects of many different environmental factorson variation in head height, a continuouslyvarying quantitative trait of Daphnias exoskele-ton (Sarkar 1999). He is credited with coiningthe term Reaktionsnorm (Schlichting & Pigliucci1998), an idea that languished for decades be-
fore interest in phenotypic plasticity was rekin-dled during the mid-1960s and 1970s. Sincethen, the concept of the reaction norm has of-ten been used alongside other ecological andquantitative genetic techniques. It has been ahelpful unifying concept for empiricists andtheoreticians studying traits that exhibit phe-notypic plasticity (Via & Lande 1985; Endler1986; De Jong 1995; Rose & Lauder 1996).
Often, research in phenotypic plasticity hasprogressed by zooming out, ignoring the de-tails of the genes underlying a reaction norm.Instead, such work typically focuses on a par-ticular plastic trait or traits, examining how se-lection acts on them or investigating their effecton ecological performance. With this perspec-tive, many decisions must be made in translat-ing the phenomenon of phenotypic plasticityinto quantifiable terms. Often, models treat theplasticity of a trait as itself a complex, quantifi-able trait. Then, variation in traits and in theplasticities of the traits can be conceptualizedinto discrete, hierarchical categories. The firstissue is whether the trait is absent or present.If the trait is present, it is necessary to examinewhether the traits expression is constitutive orinducible (i.e., expressed in some environmentsbut not others).
Beyond categorizing a plastic trait as con-stitutive or inducible, it is often desirable toquantify inducibility by scoring trait expressionquantitatively across two or more environ-ments, sometimes along a gradient. Quantifi-cation of trait expression in multiple environ-ments can be useful for translating a traitsplasticity into a trait in and of itself, a trait thatis necessarily quantitative. Quantifying plastic-ity as a continuous trait has been carried outby calculating measures of spread (e.g., vari-ance, coefficient of variation) (Schlichting 1986)or by using the raw or standardized differ-ence between contrasting environments (Fal-coner 1990; Ungerer et al. 2003). In some situ-ations, the absolute value of differences is used.This may be an appropriate choice because itis clear that the direction or pattern of plas-ticity is bidirectional (i.e., passive phenotypic
46 Annals of the New York Academy of Sciences
plasticity, for which the range of responses isof greater interest than the directionality). Orit may be used because of insufficient knowl-edge about the details of a given syndrome ofplasticity (Scheiner & Berrigan 1998; Dewitt &Scheiner 2004; van Kleunen & Fischer 2007).Researchers who already know that the mag-nitude of plasticity varies, and that it typicallyshifts in one direction (i.e., active phenotypicplasticity), tend to quantify a trait in two en-vironments and to use the difference in traitvalues between environments as a metric ofplasticity. In such systems, plasticity can alsobe examined across an environmental gradi-ent, followed by fitting a reaction norm functionand using the functions parameters (e.g., slope,intercept, higher-order curvature) to quantifyplasticity (Finlay & Wilkinson 1963; Gibert et al.1998; Stratton 1998; Stinchcombe et al. 2004;Kingsolver et al. 2007). Any quantification ofplasticity allows for ranking genotypes in termsof greater or lesser magnitude or level ofplasticity and for analyzing plasticity as itself aquantitative trait.
Both theorists and empiricists have had tomake decisions about these and other method-ological details, which sometimes assume sub-stantial differences in the underlying biology orecological function. This is an essential step re-quired before developing or applying modelsaddressing whether the evolution and mainte-nance of plasticity depends on the details of theenvironment. Intuitively, and consistent withmany theoretical models, loss of plasticity andgreater stability are generally favored in morestable environments, whereas plasticity is gen-erally favored by heterogeneous or fluctuatingenvironmentsbut outcomes can be complexdepending on the reliability of the cue and/orthe sensory detection mechanism that organ-isms use to detect environmental fluctuations,by time lags, by details of the plasticity-elicitingand selective environments, and by costs as-sociated with plastic phenotypes (van Tien-deren 1991; Moran 1992; Scheiner & Callahan1999; Sultan & Spencer 2002; Zhang 2006;Kingsolver et al. 2007).
Indeed, as work in this vein has progressed,it has often been noted that heterogeneity inthe environment is ubiquitous (e.g., Lechowicz& Bell 1991), yet plasticity is neither univer-sal nor infinite. Indeed, many traits are stableor canalized rather than plastic, and the exis-tence of substantial genetic diversity tells us thatno genotype has evolved plastic traits so flex-ible that it can dominate in all environments(Tollrian & Harvell 1999; Pigliucci 2001). The-orists and empiricists have therefore often em-phasized benefits and costs to account forwhy plasticity versus stability may be selectedin different ecological contexts. Unfortunately,definitions and usage of the term costs arefrustratingly idiosyncratic. Sifting through themany reports with phenotypic plasticity inthe title or keyword list, one will find some ar-guing that costs contribute to natural selec-tion favoring plasticity, others arguing the exactopposite, and some even arguing both. In thisreview, we aim to clarify some of this confusionwhile still following the lead of many theoret-ical and empirical researchers specializing inthe evolution of phenotypic plasticity. We willexamine two basic yet distinct types of costs.On the one hand are costs of the phenotypeand on the other hand are distinct costs ofplasticity that may accrue beyond costs of thephenotype.
Understanding and quantifying costs of thephenotype requires examining the evolutionaryconsequences of having one phenotype ratherthan another phenotype. That is, in a certainenvironmental context, a comparison betweendistinct phenotypes reveals different patternsof covariation between one or more quanti-fied traits and some other distinct organismalfunction. Many good examples of phenotypiccosts are found in the literature discussing an-tipredator defense traits in prey organisms. Thepotential benefit gained by expressing a de-fense trait may be offset by a costa decreasein an organismal function unrelated to avoid-ing, escaping, or resisting predators. A centralquestion is whether plastic trait expression al-lows organisms to avoid paying the price of
Callahan et al.: Phenotypic Plasticity, Costs of Phenotypes, and Costs of Plasticity 47
an inappropriately expressed trait in an envi-ronment where that trait is not advantageous.Where this is the case, an evolutionary advan-tage can be gained by shifting from expressingdefense traits constitutively to expressing themplastically only when there is risk of predation.Such costs are referred to by researchers in-vestigating many other ecological interactions,using many other terms: costs of defense, costs ofresistance, costs of induction, ecological costs, or evendirect costs (Levins 1968; Lynch & Gabriel 1987;Tollrian & Harvell 1999; Agrawal 2001). Re-gardless of such details, in this review we cate-gorize such costs as costs of the phenotype orphenotypic costs.
Conceptually distinct from costs of the phe-notype are costs of plasticity. One way to under-stand costs of plasticity is to consider genotypesthat have the same phenotype within an envi-ronment yet differ in their plastic responses to avariable environmental factor and in fitness. Insuch a situation, there is no phenotypic varia-tion, precluding phenotypic costs. Because thisis rarely the case in nature, and because thiscannot always be accomplished experimentally,plasticity costs are quantified using statisticaltools. After taking into account covariation be-tween a focal trait and a fitness-related trait, itis possible to examine residual variation in thefitness trait, variation for plasticity itself (ratherthan the trait), and covariation between thetwo (van Tienderen 1991; DeWitt et al. 1998;Scheiner & Berrigan 1998). Quantifying plas-ticity costs involves thinking about plastic traitsin a complex manner: the trait itself (as ex-pressed in one or more environments) and theplasticity of a trait (quantified using a variety ofmethods; see earlier discussion).
Although both plasticity costs and pheno-typic costs are characterized one environmentat a time, both can be examined in morethan one environment across a set of envi-ronments. Within individual environments, akey consideration is the relationship betweena traits phenotypic cost and its plasticity costbecause plasticity costs can offset phenotypic
costs. Specifically, finding that a traits plastic-ity is associated with a plasticity cost can po-tentially explain why the trait fails to be plastic(or shows suboptimal plasticity.) In this regard,plasticity costs can and should be examined inmore than one environment, because simula-tion studies suggest that plasticity costs are notlikely to counter the evolution of adaptive plas-ticity if they occur only locally but can beimportant if they occur globally (i.e., withinonly one environment across a set of environ-ments rather than in all or most environmentsacross a set of environments) (Sultan & Spencer2002).
The theoretical work of Sultan and Spencer(2002) shows that it is possible to think aboutplasticity cos...