Rethinking Phenotypic Plasticity PDF

Heredity (2015) 115, 276–284 OPEN & 2015 Macmillan Publishers Limited All rights reserved 0018-067X/15 www.nature.com/hdy REVIEW Rethinking phenot...

Heredity (2015) 115, 276–284 OPEN & 2015 Macmillan Publishers Limited All rights reserved 0018-067X/15 www.nature.com/hdy REVIEW Rethinking phenotypic plasticity and its consequences for individuals, populations and species A Forsman Much research has been devoted to identify the conditions under which selection favours flexible individuals or genotypes that are able to modify their growth, development and behaviour in response to environmental cues, to unravel the mechanisms of plasticity and to explore its influence on patterns of diversity among individuals, populations and species. The consequences of developmental plasticity and phenotypic flexibility for the performance and ecological success of populations and species have attracted a comparatively limited but currently growing interest. Here, I re-emphasize that an increased understanding of the roles of plasticity in these contexts requires a ‘whole organism’ (rather than ‘single trait’) approach, taking into consideration that organisms are integrated complex phenotypes. I further argue that plasticity and genetic polymorphism should be analysed and discussed within a common framework. I summarize predictions from theory on how phenotypic variation stemming from developmental plasticity and phenotypic flexibility may affect different aspects of population-level performance. I argue that it is important to distinguish between effects associated with greater interindividual phenotypic variation resulting from plasticity, and effects mediated by variation among individuals in the capacity to express plasticity and flexibility as such. Finally, I claim that rigorous testing of predictions requires methods that allow for quantifying and comparing whole organism plasticity, as well as the ability to experimentally manipulate the level of and capacity for developmental plasticity and phenotypic flexibility independent of genetic variation. Heredity (2015) 115, 276–284; doi:10.1038/hdy.2014.92; published online 8 October 2014 INTRODUCTION Does plasticity promote or hinder evolution and speciation? Why does The focus of this review is ‘whole organism’ (rather than ‘single trait’) plasticity vary among populations and species? Is plasticity adaptive? plasticity, how it may affect the ecological success of individuals, What are the costs of plasticity? Do genes typically act as ‘leaders’ or populations and species, and how to rigorously test predictions from ‘followers’ in evolution? What is the relative contribution of plasticity theory regarding its consequences. Knowledge of the causes, mechan- versus evolution (via modifications of allele frequencies) to population istic underpinnings and consequences of phenotypic plasticity and the differentiation? What are the ecological conditions that promote the capacity of a genotype to produce different phenotypes in response to evolution and maintenance of plasticity? Some issues, such as the environmental variation is crucial for a better understanding of the genetic underpinnings of plasticity and gene-by-environment interac- evolution and maintenance of biodiversity (Bradshaw, 1965; Sultan, tions, have been settled or superseded by new questions and 2000; Agrawal, 2001; Pigliucci, 2001; Meyers and Bull, 2002; Bolnick approaches (Pigliucci, 2005). Plasticity can be considered at the level et al., 2003; Booth and Grime, 2003; Sultan, 2004; Miner et al., 2005; of genes, individuals, and populations (see, for example, Carroll and Pigliucci, 2005; Gray and McKinnon, 2007; Whitlock et al., 2007; Corneli, 1995; Colbourne et al., 1997; Pigliucci et al., 2003; Nussey Forsman et al., 2008; Naeem et al., 2009; Whitman and Agrawal, 2009; et al., 2007; Chun, 2011; Brommer, 2013; Araya-Ajoy and Dinge- Pfennig et al., 2010; Reed et al., 2010; te Beest et al., 2011; Violle et al., manse, 2014), but there are also studies based on comparisons of 2012; Wund, 2012; Snell-Rood, 2013). From having been considered plasticity among species (see, for example, Thaler and Karban, 1997; primarily as nuisance in evolutionary biology, plasticity research has Pigliucci et al., 1999; Pollard et al., 2001; Davidson et al., 2011). Here, I grown tremendously (Scheiner and DeWitt, 2004), from o10 papers focus primarily on the consequences for individuals and populations published per year before 1983 to nearly 1300 papers in 2013 of whole organism developmental plasticity and phenotypic flexibility. (Figure 1). To what extent has this growing attention, appreciation An enhanced knowledge of the population-level consequences of of the potential importance of plasticity and increased scientific output interindividual genetic and phenotypic variation may increase our been accompanied by a similar increase in our understanding and ability to understand the ecological dynamics of natural populations, knowledge of the causes and consequences of plasticity? and ultimately to develop more informed management plans for Much research has been devoted to unravel how plasticity may protection and restoration of threatened species and biodiversity influence and contribute to diversity among individuals, populations (Kendall and Fox, 2002; Frankham et al., 2010; Wennersten and and species. Key questions in this area include, but are not limited to: Forsman, 2012). Ecology and Evolution in Microbial Model Systems, EEMiS, Department of Biology and Environmental Sciences, Linnaeus University, Kalmar, Sweden Correspondence: Professor A Forsman, Ecology and Evolution in Microbial Model Systems, EEMiS, Department of Biology and Environmental Sciences, Linnaeus University, Barlastgatan 11, SE-391 82 Kalmar, Sweden. E-mail: [email protected] Received 27 March 2014; revised 20 August 2014; accepted 26 August 2014; published online 8 October 2014  Rethinking plasticity and its consequences A Forsman 277 Table 1 List of plasticity-related terms and concepts, arranged in the order they appear in the text Phenotypic plasticity Gene by environment interaction Developmental plasticity Phenotypic flexibility Norms of reaction Induced responses Intraindividual plasticity Induced differentiation Active plasticity Passive plasticity Figure 1 Trends in research output on plasticity. Figure shows number of Inducible defences publications per year up to December 2013. Figure is based on data Phenotypic flexibility extracted from a topic search for ‘phenotypic plasticity’ OR ‘developmental Reaction norms plasticity’ OR ‘phenotypic flexibility’ OR ‘behavio*ral plasticity’ conducted on Maternal effects 21 March 2014 from ISI Web of Science. The literature search yielded Cross generational plasticity 11 822 papers published between 1967 and December 2013. More than Reversible changes within individuals 1000 papers are review articles. Labile traits Behavioural plasticity Activational plasticity FROM CAUSES TO POPULATION-LEVEL CONSEQUENCES OF Irreversible developmental plasticity PLASTICITY Window of sensitivity In recent years, there has been an increased interest in the questions of Multivariate trait plasticity how interindividual variation and plasticity influence the performance The list is nonexhaustive, and additional terms and concepts can be found in the plasticity and ecological success of individuals, populations and species (Sultan, literature. 2000; Agrawal, 2001; Pigliucci, 2001; Bolnick et al., 2003; Miner et al., 2005; Forsman et al., 2008; Hughes et al., 2008; Chevin et al., 2010; interindividual phenotypic variation resulting from induced responses Pfennig et al., 2010; Violle et al., 2012; Wennersten and Forsman, (which could also arise in the absence of genetic variation for plasticity 2012). Overall, theoretical models agree that phenotypically and if individuals utilize different microhabitats). genetically more variable populations are predicted to be associated Developing, summarizing and comparing theoretical models and with broader niches, reduced intraspecific competition, increased their predictions (see, for instance, Table 1 in Wennersten and productivity and population growth rate, decreased vulnerability to Forsman, 2012) are necessary and important tasks. Given the environmental changes, dampened fluctuations in population size, development during the past decades, the time is now ripe for increased establishment success, increased invasiveness, larger distri- empirical evidence to catch up with theoretical predictions concerning bution ranges, decreased extinction risk and increased rate of the consequences of plasticity. This is challenging, because, as argued speciation as compared with less variable populations (reviewed by below, to empirically evaluate the predicted consequences (and other Forsman et al., 2008; Wennersten and Forsman, 2012 and references issues) of plasticity requires methods allowing for quantifying and therein). Wennersten and Forsman (2012) systematically evaluate comparing ‘single trait’ as well as ‘whole organism’ plasticity. In whether the consequences of interindividual variation are likely to addition, I claim that rigorous testing of predictions requires that we be similar or different depending on the nature of the source of can experimentally manipulate the levels of or the capacity for variation. Despite some exceptions with regard to temporal and spatial plasticity. scales, the population-level consequences listed above are, at first glance, largely similar regardless of whether the variation stems from WHAT IS PLASTICITY? genetic polymorphism (allelic variation at coding loci), plasticity or As pointed out by others, the concept of phenotypic plasticity is randomized phenotype switching (see Table 1 in Wennersten and deceptively simple, and it has been defined in numerous ways by Forsman, 2012). different authors (see, for instance, Box 1 in Whitman and Agrawal, The overall agreement with regard to consequences is in part 2009). One apparent form of intraindividual plasticity, common to illusory, because the mechanisms that mediate the consequences of most if not all multicellular organisms, is the pronounced phenotypic plasticity versus polymorphism are sometimes different (for a discus- differentiation among cells found in different organs and types of sion and examples see Wennersten and Forsman, 2012). Furthermore, tissue (Sánchez Alvarado and Yamanaka, 2014). Cells that comprise predictions are sometimes similar because models on the conse- blood, bone, nerve and muscle within a single individual are quences of plasticity build in part on the assumption that there are phenotypically extremely different, despite that they share an identical heritable differences among genotypes in norms of reaction (how the (at least close to) set of genes and alleles. Such induced differentiation phenotypic expression of genotypes change along an environmental has previously been discussed from a plasticity perspective within the gradient), in which case the distinction between genetic polymorphism domains of ecology and evolutionary biology (see, for example, Sarà, and plasticity is debatable (West-Eberhard, 2003; Leimar, 2009; 1996; Newman and Müller, 2000; Schlichting, 2003). Shuster, 2010; Wennersten and Forsman, 2012). The consequences Plasticity is oftentimes defined as the ability of a single genotype to of plasticity for the ecological success of populations and individuals exhibit a range of different phenotypes in response to variation in the may also differ depending on whether one is concerned with variation environment. The term phenotypic plasticity is used in studies that among individuals in the capacity to express plasticity, or with concern and report on phenomena that are in fact rather different, Heredity  Rethinking plasticity and its consequences A Forsman 278 and alternative terms are sometimes used for one and the same threshold responses regulated by complex mechanisms including phenomenon (Piersma and Drent, 2003; Whitman and Agrawal, 2009; polygenic effects and shifts induced by continuously distributed Stamps and Groothuis, 2010; Brommer, 2013; Snell-Rood, 2013). The underlying cues (Stearns, 1989). A candidate example is wing same or similar concepts are sometimes also used for different polymorphism, the co-occurrence of flight-capable individuals that phenotypic dimensions, such as morphology, physiology, life history possess fully developed functional wings and flightless individuals with and behaviour, and for situations when the phenotype changes in only partially developed or no wings that in some insect species seems response to variation in either the external or the internal environ- to be regulated by juvenile hormone titres (Zera, 2003; Roff and ment. On one hand, the tendency to apply the same concept to Fairbairn, 2007; Schwander and Leimar, 2011). Plasticity can also different types of context-dependent phenotypic variation can be involve mechanisms that operate between or across generations. In justified on the grounds that science may benefit from unifying, quantitative genetics and evolutionary biology, when the environment common theoretical frameworks. On the other hand, it is sometimes responsible for the induced phenotypic response consist of the justified to use different concepts. Given the rich terminology (female) parent, the developmental plasticity is usually referred to as (Table 1), however, authors should take great care to clarify how maternal effects (Roff, 1997; Mousseau and Fox, 1998) or cross they interpret and use the plasticity concept and related terms to avoid generational plasticity. misunderstandings, because people vary in what they think plasticity is The term ‘phenotypic flexibility’ seems to be used primarily by and what it is not. researchers who focus on intraindividual plasticity, that is, reversible changes within individuals of labile, context-dependent physiological, Active versus passive plasticity morphological and life-history traits (Piersma and Drent, 2003). One distinction worth mentioning in this context is that between Examples include metabolic and endocrine switches, shifts in the sizes active and passive plasticity (Scheiner, 2006; Kurashige and Callahan, of body parts and organ systems in relation to reproductive condition 2007; Whitman and Agrawal, 2009), because there might be differ- and metabolic demand, changes in colour patterns in relation to ences in the way that these two aspects of plasticity affect the ecological seasonality, changes within individuals among years in the timing of success of individuals and populations. Active plasticity is used for reproductive activities in response to weather conditions and changes predominantly anticipatory, and often highly integrated, phenotypic in number of eggs or offspring between sequential reproductive events. changes in response to some environmental cue or signal, and reflect Phenotypic flexibility is also applied to changes in behavioural traits modifications of developmental pathways and regulatory genes. In (Dingemanse et al., 2010; Stamps and Groothuis, 2010; Tuomainen active plasticity, such as in the case of wing-length polymorphism in and Candolin, 2011), for instance, as a result of learning and some species of insects (Roff and Fairbairn, 2007; Schwander and experience or adjustments depending on the presence or absence of Leimar, 2011), the magnitude of the induced phenotypic response(s) is predators, and encompasses both developmental behavioural plasticity not necessarily correlated with the strength of the environmental and activational plasticity (for a thorough discussion see Snell-Rood, signal (Scheiner, 2006). However, graded responses are also relatively 2013). Despite the flexible nature of many behavioural traits, there is common for active plasticity. For example, the magnitude of inducible also a tendency of individuals to display consistency through time. In defences in prey may increase as the number of predators, or the the behavioural plasticity literature, there is a growing interest in the amount of cue produced by predators, increases. Passive plasticity, on causes and consequences of such consistency within individuals and the other hand, may stem from direct environmental influences on repeatable variation among individuals, often referred to as animal chemical, physiological and developmental processes, and is generally personalities or ‘behavioural syndromes’, for instance in the form of not considered anticipatory, but a mere consequence of the environ- shyness versus boldness in different types of behaviour and across ment, such as stunted growth owing to low resource levels. In the case environmental contexts (Stamps and Groothuis, 2010; Brommer, of passive plasticity, when the environment acts directly on the 2013; Araya-Ajoy and Dingemanse, 2014). expression of the trait, phenotypic changes are often proportional to environmental differences (Scheiner, 2006). Active phenotypic plasti- Is plasticity distinct from genetic polymorphism? cities are often (unlike ‘truly’ passive plasticities) considered adaptive, There are still articles published (including some of my own) that but the distinction between the two is not always clearcut (Scheiner, contain phrasings and arguments along the lines of genetics versus 2006; Whitman and Agrawal, 2009). plasticity that might suggest that the authors do not consider plasticity a property of the genotype. There are probably examples of Developmental plasticity versus phenotypic flexibility intraindividual reversible phenotypic flexibility and behavioural plas- The term ‘developmental plasticity’ is used by many researchers who ticity that are only loosely connected to genetics. Plasticity is not focus on irreversible phenotypic variation in traits of individuals (or equivalent to genetic polymorphism, and their evolutionary dynamics genotypes) that result from environmentally induced modifications of can differ considerably (Day and Bonduriansky, 2011; Frank, 2011; development and growth. Some traits remain largely fixed after Saito et al., 2013). However, irreversible developmental plasticity is not maturity, such as structural body size in some unitary organisms, fundamentally different from genetic determinism, except for the the number of vertebrae in limbed vertebrates and various morpho- environment dependence of the expression of the phenotypic state, logical defence structures induced by the presence of predators. and they are best interpreted and analysed within a common, Reaction norms (or norms of reaction) that describe the association quantitative genetics, framework (Agrawal, 2001; Pigliucci, 2001; linking the phenotypic expression of genotypes to an environmental West-Eberhard, 2003; Jablonka and Lamb, 2006; Leimar et al., 2006; gradient, and genotype by environment interactions that refer to the Day and Bonduriansky, 2011; Wennersten and Forsman, 2012). Most differential phenotypic responses of alternative genotypes, are key phenotypic traits display a certain amount of plasticity, and plasticity components in this field (Stearns, 1989; Roff, 1997; Lynch and Walsh, includes genetic components (Stearns, 1989; Pigliucci, 1996, 2001; 1998; Pigliucci, 2001; West-Eberhard, 2003). Developmental plasticity Pigliucci and Preston, 2004). Indeed, the existence of crossing norms is not restricted to traits that display quantitative variation, and it can of reaction, such that different genotypes display different phenotypic result in discrete phenotypic classes that represent developmental responses to environmental change, reflects an underlying genetic Heredity  Rethinking plasticity and its consequences A Forsman 279 polymorphism (Stearns, 1989; Pigliucci, 2001; West-Eberhard, 2003). considerable variation in the number of vertebrae, both among species This means that population-level consequences of plasticity predicted and among individuals within populations (Arnold, 1988; Lindell by theory are largely mediated by the same mechanisms as are those of et al., 1993; Lindell, 1994). Vertebral number reflects the combined genetic polymorphisms (for exceptions see Wennersten and Forsman, effects of heritable (additive) genetic variation and developmental 2012). plasticity in response to temperature conditions during early embryo- nic development, and unlike growth rate and body size it does not WHAT IS A TRAIT? change during the rest of the life of the individual (Arnold, 1988; Not all types of traits can be straightforwardly assigned to either of the Lindell et al., 1993; Shine, 2000 and references therein). Because above categories of plasticity. For instance, the size and shape of snakes are gape-limited predators that swallow their prey in one piece, antlers in mammals of the family Cervidae, such as deer, is an example their foraging success depends on body size (Forsman and Lindell, of irreversible developmental plasticity, but new antlers are grown each 1993; Forsman, 1996a). year, and the antlers of an individual can change in both size and Through its effect on locomotor capacity and speed (Arnold and shape among years. Similarly, the size and colouration of feathers in Bennett, 1988), there is also potential for vertebral number to birds remain largely fixed after feathers are fully grown, but can indirectly influence foraging success and growth rate. Snakes are change within individuals between moults. This raises the question of ectothermic, and their growth rates depend strongly on body whether the antlers of a deer, the plumage of a bird or aspects of temperature, as do virtually all aspects of their physiology and behavioural and life-history characters as expressed on different behaviour, including foraging activities (Huey and Kingsolver, 1989). occasions by the same individual should be considered as one or as Body temperature of snakes is in turn influenced by behavioural different traits. One way to address such intraindividual plasticity is to thermoregulation mediated via shifts in bodily postures and shuttling quantify, compare and model individual reaction norms based on between microhabitats; examples of reversible phenotypic flexibility longitudinal data (Nussey et al., 2007; Araya-Ajoy and Dingemanse, and behavioural plasticity (Stevenson, 1985b; Forsman, 1995). Body 2014). In modular organisms, phenotypic responses to environmental temperature of snakes and other ectothermic organisms is also cues can be differentiated and restricted to certain body compart- influenced by external weather conditions, and by body colouration ments, such as size and shape of leaves subjected to sun-exposed and body size, all of which affect the rate at which solar radiation is versus shaded environments (Pigliucci et al., 1999, 2003), and aerial converted into body heat as well as equilibrium body temperature versus aquatic leaves in some plants (Bruni et al., 1996; Sultan, 2003). (Stevenson, 1985a; Forsman, 1995; Forsman et al., 2002; Ahnesjö and Interestingly, this enables the individual to be a generalist, and may be Forsman, 2006; Karpestam et al., 2012). This example illustrates that of particular importance for sessile organisms that cannot choose or to apply the plasticity concept(s) to single ‘traits’ (for example, body move to a more suitable environment. size) as a means to increase our understanding of organismal design As another case in point, consider the plethora of factors that and differentiation among individuals and populations can be a influence growth rate and body size in snakes (Figure 2). Snakes have daunting endeavour (Figure 2). indeterminate growth, meaning that they continue to grow more or less throughout life, although at a rate that decreases with increasing FROM SINGLE TRAITS TO A WHOLE ORGANISM PERSPECTIVE body size and age, and with males or females growing larger adult It can be argued that ‘traits’ do not really exist, except as mental body sizes depending on species (Shine, 1991). Their growth rates are constructions to aid communication (Fristrup, 2001). Indeed, indivi- flexible and influenced by the internal environment, including genetic duals are developmentally, functionally and phenotypically integrated makeup and number of vertebrae (Lindell et al., 1993; Shine, 2000), as complex units (Olson and Miller, 1958; Schlichting and Pigliucci, well as by the external environment, for instance in the form of prey 1998; Pigliucci and Preston, 2004; Valladares et al., 2007; Piersma and availability (Forsman and Lindell, 1996; Lindell and Forsman, 1996; van Gils, 2011). Within an individual, homeostasis, canalization or the Forsman, 1996b). Unlike vertebrate taxa with limbs, snakes display absence of plasticity (or a flat reaction norm for a genotype) in a focal Figure 2 Interdependence among phenotypic dimensions, plasticity, flexibility and environmental influences jointly affect body size in snakes. Schematic representation of the many ways by which different phenotypic dimensions interact and are influenced by internal and external environmental factors and how they may jointly contribute to within- and among-individual variation in growth rate and body size of snakes. This example illustrates that individuals are complex integrated units that cannot be decomposed into a suite of independent ‘traits’, and that variation in a given phenotypic dimension can be influenced by combinations of both genes, irreversible developmental plasticity and by reversible phenotypic flexibility in response to changes along different environmental factors. See text for details. Heredity  Rethinking plasticity and its consequences A Forsman 280 trait must reflect some sort of buffering mechanism and plasticity in environmental cues. This is because the population or species under some other trait(s) (Pigliucci and Preston, 2004; Whitman and investigation may potentially show plasticity in response to environ- Agrawal, 2009). Such buffering can be mediated by a flexibility of mental cue(s) that have not yet been investigated, or have a restricted physiological processes, developmental pathways and by behavioural window of sensitivity not yet tested (Pigliucci, 2001; West-Eberhard, adjustments (Figure 2). Although developmental plasticity and phe- 2003). Furthermore, the outcome of plasticity experiments conducted notypic flexibility can enable individuals to change their phenotype under laboratory conditions may not accurately reflect the role of according to the environment, mobile organisms may also have the plasticity under different and usually more complex and challenging opportunity to change their environment according to phenotype by circumstances in the wild (Nussey et al., 2007; Valladares et al., 2007; means of matching habitat choice (Edelaar et al., 2008; Karpestam Fox and Reed, 2010). It may not be possible to reliably compare and et al., 2012). This raises the questions of whether it is meaningful and rank individuals, populations or species with regard to some overall possible from a whole organism perspective to classify individuals, level of or capacity for whole organism plasticity. However, compar- populations or species as being either plastic or non-plastic isons can be done at the level of specific phenotypic dimensions and If one takes into consideration the entire integrated suite of with regard to how they respond to changes along the gradient of one physiological, behavioural, morphological and life-history phenotypic or a few specified environmental factors. In lieu of estimates of whole dimensions, it can be argued that there is no such thing as a non- organism plasticity, multiple phenotypic dimensions can be examined, plastic individual, because lack of or low levels of plasticity in one trait modelled and compared simultaneously by either using multivariate is generally compensated for or made possible by higher plasticity or statistical analysis or using composite measures of plasticity based on flexibility along some other phenotypic dimension(s). This realization averages across traits or dimension reducing techniques (such as is important when it comes to making comparisons, evaluating principal component analysis) as a means to inform about differences hypotheses and testing predictions pertaining to the fitness conse- in the nature and magnitude of plasticity among individuals, popula- quences of plasticity for individuals and populations. To avoid tions and species (see, for example, Carroll and Corneli, 1995; misunderstandings, any inferences and conclusions with regard to Pigliucci et al., 1999; Pollard et al., 2001; Nussey et al., 2007; Chun, causes and consequences of plasticity should be restricted to the 2011; Davidson et al., 2011; Araya-Ajoy and Dingemanse, 2014). particular phenotypic dimension(s), aspects of plasticity and environ- mental cues(s) that have been investigated, and not extended to HOW CAN HYPOTHESES AND PREDICTIONS REGARDING general statements regarding plasticity. CONSEQUENCES OF PLASTICITY BE TESTED? To put the predictions about plasticity to empirical tests, we must be COMPARING LEVELS OF PLASTICITY AMONG INDIVIDUALS, able to quantify, compare and ultimately manipulate the level of and POPULATIONS AND SPECIES capacity to express plasticity. This is true not only for the proposed Multicellular organisms are complex combinations of phenotypic population-level consequences (Wennersten and Forsman, 2012); the properties that display more or less plasticity (Bradshaw, 1965; need to quantify, compare and manipulate plasticity also applies if we Sultan, 2000; Pigliucci, 2001; Schlichting, 2003; West-Eberhard, want to investigate, for example, whether plasticity influences fitness, 2003; Pigliucci and Preston, 2004; Araya-Ajoy and Dingemanse, whether it is adaptive and whether it is costly (Tonsor et al., 2013). 2014). One should therefore not expect plasticity to be correlated across phenotypic dimensions or environments. A given genotype may Associations based on observational data may be informative but show a plastic response (a non-flat reaction norm) of one or some do not reveal causation particular dimension(s) of the phenotype in response to a certain Indications of costs or benefits of plasticity might be gained from environmental factor, whereas other phenotypic dimensions are not comparisons of performance of different genotypes or between affected by the same environmental factor. Similarly, a given genotype populations subjected to different environmental conditions (Wund, or phenotypic dimension may display plasticity in response to changes 2012). Similarly, associations of variation in single- or multivariate along the gradient of one environmental factor, whereas changes along trait plasticity with changes along environmental gradients can inform other environmental gradients do not affect the expression of the same about which factors and conditions might promote the evolution of genotype nor influence its associated phenotypic variability (Valladares induced phenotypic variation. It is also possible to test for associations et al., 2007). Conclusions regarding the consequences of plasticity of plasticity with fitness in the wild, but this requires tedious analyses, responses and gene by environment interactions therefore depend on and interpretation of results is not straight forward (Nussey et al., the choice of trait(s) as well as on the choice of environmental 2007; Brommer, 2013). For instance, Araya-Ajoy and Dingemanse covariate(s) (Valladares et al., 2007; Brommer, 2013). Assessments of (2014) proposed an analytical approach that allows for studying (co) plasticity are typically focussed on traits with established or a priori variation in labile behavioural character complexes both within and functional significance and how they respond to changes along some among individuals using multivariate mixed-effects models. Their ecologically important environmental gradient. Consequently, there is approach resembles to some extent the one put forward by Nussey a risk with a reductionist approach that we might arrive at a biased et al. (2007) for quantifying, comparing and partitioning variation view of, and perhaps even overestimate, the importance of plasticity. among individuals and populations in reaction norms of labile life- To improve our understanding of the evolutionary dynamics of history traits based on longitudinal data from natural populations. plasticity and its consequences, it is necessary to also identify those Comparisons among populations that inhabit different environments environmental factors that do not elicit plastic responses, as well as the may help identify potential drivers of plasticity evolution and suggest ecological settings under which plasticity is less beneficial. how plasticity can contribute to evolutionary differentiation within A plastic response in a given phenotypic dimension can be species (see, for example, Carroll and Corneli, 1995; Pollard et al., demonstrated experimentally. However, to reliably classify genotypes, 2001; Nunes et al., 2013). On a larger scale, phylogeny-based populations or species as being non-plastic is complicated because it is comparative analyses can be used to infer about the role of plasticity impossible to determine with certainty that observable phenotypic for evolutionary diversification among species and for speciation (see, variation among individuals is not influenced at all by responses to any for example, Colbourne et al., 1997; Thaler and Karban, 1997; Heredity  Rethinking plasticity and its consequences A Forsman 281 Pigliucci et al., 1999; Price et al., 2003; Pfennig et al., 2010; Schwander tits (Parus major) and conclude that the most important way that birds and Leimar, 2011). However, with a whole organism perspective on can cope with climate change is their evolved ability to adjust their plasticity (that is, acknowledging that homeostasis in one particular behaviour and seasonal timing of reproductive activities depending on phenotypic dimension is mediated by plasticity or flexibility in other spring temperature and abundance of a critical food resource, with dimension(s)), it is difficult to envisage how to perform such extinction risk being 500 times higher in the absence of plasticity. comparisons and demonstrate such associations—let alone to establish Modelling approaches suggest that developmental variability and causation. learning can enhance nonheritable phenotypic variation and, by smoothening of multipeaked landscapes that relate genotypes to How to manipulate plasticity in order to establish causation? fitness, this can in principle affect both the course and the rate of Studies based on observational approaches can offer important evolution to a fitness peak, and it can do so in changing as well as in insights, generate hypothesis and testable predictions and uncover ‘fixed’ environments (see, for example, Ghalambor et al., 2007; Frank, patterns and associations in accordance or disagreement with predic- 2011; Saito et al., 2013). However, although plasticity can accelerate tions. However, demonstrating causal relationships and mechanisms evolutionary rate, there are indications that it may decrease the average linking either variation in the capacity for plasticity itself or plasticity- fitness (Saito et al., 2013). induced phenotypic variation to aspects of individual or population In the case of developmental plasticity, it has been stated that it may fitness is complicated because it requires experimental manipulation, enhance establishment success, promote invasiveness, decrease vulner- replication and controlled comparisons (Forsman, 2014). ability to environmental change and reduce extinction risk because it To experimentally manipulate the level of or capacity for plasticity allows for individuals (or their progeny) to develop phenotypes that seems very challenging, at least if one aims to test for effects of the are well suited to novel conditions without first undergoing local capacity to express plasticity or flexibility (independent of genetic genetic adaptation through natural selection (see, for example, Sultan, variation), and if one is concerned with whole organism rather than 2000; Pfennig et al., 2010). Forsman (2014) reported on the results of single trait plasticity. Artificial selection or genetic engineering might a meta-analysis of experimental manipulation studies of plants and be used to increase or reduce levels of plasticity-induced phenotypic animals, demonstrating that greater genetic and phenotypic variation variation (Krebs and Feder, 1998; Feder, 1999). However, interpreta- among individuals included in founder groups contribute to increased tion of such manipulation studies is not straight forward, because of establishment success, but that study did not aim to evaluate the the potential for pleiotropy and epistasis (Lynch and Walsh, 1998), effects of plasticity on establishment. The reason for this exclusion was and because changes in plasticity of the focal trait may be accom- that, to my knowledge, there are as yet no studies that have panied by increased or decreased plasticity in buffering traits. experimentally manipulated the capacity for plasticity to investigate Phenotypic engineering based on hormonal treatments offers another whether and how this might affect establishment and population possibility to experimentally manipulate the phenotypic expression of persistence. In contrast, Davidson et al. (2011) reported on the results plastic and flexible traits (Sinervo and Huey, 1990; Ketterson et al., of a meta-analysis that indicate that invasive plant species display 1996), but again interpretation of results is complicated because higher phenotypic plasticity compared with co-occurring, closely hormones can have a multitude of cascading and interacting effects related, noninvasive species. They used for their comparisons both on organismal functioning. To test for effects and consequences of separate traits and a composite measure of species plasticity based on plasticity based on comparisons between experimental treatments that means across different traits. On a larger scale, it has been suggested consist of unmanipulated individuals with naturally high versus low plasticity is equally problematic, because differences in plasticity that plasticity promotes evolutionary diversification and speciation between treatments would not be independent of genetic variation. (Price et al., 2003; West-Eberhard, 2003; Pfennig and McGee, 2010; Chevin et al. (2013) provide a discussion and offer suggestions on the Pfennig et al., 2010; Pigliucci, 2010), but again experimental evidence related issue of experimental evolution of plasticity. seems to be lacking. The role of plasticity in some contexts should be contingent upon POPULATION-LEVEL CONSEQUENCES OF PLASTICITY the spatial and temporal scales of environmental heterogeneity and REVISITED change, relative to the dispersal capacity and generation time of the In view of what has been said above, is there any rigorous evidence in organisms (Levins, 1968; Frank and Slatkin, 1990; Saito et al., 2013). It support of the predictions (Table 1 in Wennersten and Forsman, 2012 is conceivable that if there is a substantial time lag between exposure to and references therein) that plasticity should promote the ecological the environmental cue and the expression of the induced response, and evolutionary success of populations and species? It is important in selection may drive the population to extinction before the appropriate this context to distinguish between effects mediated by variation in the phenotype has been realized (Wennersten and Forsman, 2012). Costs capacity to express plasticity and flexibility versus consequences associated with such time lags are likely to be manifest most strongly associated with a higher (or lower) level of interindividual phenotypic for irreversible developmental plasticity when the induced change is variation resulting from plasticity. not realized until the next generation. This hypothesis could poten- The buffering effect of plasticity-induced phenotypic variation tially be evaluated experimentally by first using a split-brood design, against environmental change should apply primarily to labile or exposing half of the siblings to a range of environmental conditions to flexible traits, and to fine-grained environments where the changes are increase the level of interindividual phenotypic variation, and the other predictable (Wennersten and Forsman, 2012). Recent reviews and half to homogeneous conditions, and then comparing the establish- discussions of behavioural flexibility are largely in accordance with this ment success, population dynamics and persistence of phenotypically prediction (Tuomainen and Candolin, 2011; Snell-Rood, 2013), but highly variable versus less variable founder groups. This would not the evidence is based almost exclusively on observational data and answer the question of whether the capacity for plasticity buffers theoretical modelling. For instance, Vedder et al. (2013) report on a against environmental change, but would indicate whether standing quantitative assessment of the importance of plasticity in adaptation to phenotypic variation resulting from plasticity promotes ecological climate change based on a long-term population study of wild great success of populations. Heredity  Rethinking plasticity and its consequences A Forsman 282 Whether or not plasticity is beneficial for fitness of individuals and  To improve our understanding of the evolutionary dynamics of viability of populations is also contingent on how reliably the cues plasticity and its consequences, and to avoid overestimating its predict future environmental conditions and selective regimes. For importance, it is necessary to identify also those phenotypic instance, Reed et al. (2010) presented results of a stochastic individual- dimensions that are less likely to express plasticity or flexibility, based model and found that demographic consequences of plasticity those environmental factors that do not elicit plastic responses as depend in a complex, nonadditive way on the reliability of environ- well as the ecological settings under which plasticity is less beneficial. mental cues and the magnitude of environmental fluctuations. When  Past and current research, based on theoretical modelling and environmental variation was highly unpredictable, strong plasticity observational data, indicates that plasticity may either promote or increased rather than decreased extinction risk (Reed et al., 2010). See impair ecological success of populations, depending on environ- also Chevin et al. (2013) for a discussion of this issue. mental conditions. However, firm evidence to this effect is lacking. Taken together, it seems that plasticity may either promote or  To demonstrate causal relationships and mechanisms linking impair ecological success of populations, depending on environmental plasticity variation to aspects of individual or population fitness conditions. However, firm evidence to this effect based on experi- requires methods allowing for experimental manipulation, replica- mental manipulation approaches is lacking. Solving the problem of tion and controlled comparisons. It is also important to distinguish how to manipulate the capacity for developmental plasticity and between effects mediated by variation in the capacity to express flexibility is a daunting task, but it is crucial for continued scientific plasticity and flexibility, as opposed to effects mediated by a higher progress and to further our understanding of the many ways by which (or lower) level of interindividual phenotypic variation resulting environmental heterogeneity and change may influence the evolution from plasticity (in which case there need be no genetic variation in of genetic and phenotypic diversity at different levels of biological plasticity). organization on one hand, and to investigate how plasticity affects the  Whether and how standing phenotypic variation resulting from ecological success on the other hand. plasticity influences aspects of ecological success of populations can be experimentally investigated by first using a split-brood design to CONCLUSIONS AND FUTURE DIRECTIONS increase and decrease interindividual phenotypic variation and then  Plasticity research has grown tremendously, from o10 papers comparing for instance establishment success, population dynamics published per year before 1983 to nearly 1300 papers in 2013. and persistence of phenotypically highly variable versus less variable There has been an increased interest in the questions of how groups. interindividual variation and plasticity influences the performance  To experimentally demonstrate that interindividual genetic and and ecological success of individuals, populations and species. phenotypic variation affects ecological success of populations and  Our understanding of causes and consequences of plasticity and its species is tedious, but feasible (Hughes et al., 2008; Wennersten and role in generating and maintaining phenotypic complexity and Forsman, 2012; Forsman, 2014). However, to disentangle any effects diversity is hampered by imprecise definitions, hypothesis and of whole organism plasticity from effects owing to genetic variation, predictions, and a tendency to consider observational case studies and to rigorously investigate how variation in the capacity to express as evidence in support of predictions and confirmation of theory. plasticity affects fitness of individuals and on the ecological success Authors should take great care to clarify how they interpret and use of populations and species, requires experimental approaches yet to plasticity and related terms. be discovered. S/he who finds a solution to this problem will have a  Within an individual, homeostasis, canalization or the absence of key to considerable future scientific advance. Let the quest for this plasticity (a flat reaction norm) in a focal trait must be compensated Holy Grail begin! for by higher plasticity or flexibility along some other phenotypic dimension(s); it can thus be argued that there is no such thing as a non-plastic individual. CONFLICT OF INTEREST  Inferences and conclusions with regard to causes and consequences The author declares no conflict of interest. of plasticity should be restricted to the particular phenotypic dimension(s), aspects of plasticity and environmental cues(s) that ACKNOWLEDGEMENTS have been investigated, and not extended to general statements I thank the organizers, most especially Johan Hollander, and participants of the regarding plasticity as such, unless a whole organism approach Symposium on ‘Phenotypic Plasticity—Variation, Alteration and Speciation’ is used. held in Lund, November 2012, for inspiration. I am grateful to H Berggren,  The consequences of plasticity may differ depending on whether S Hylander, P Tibblin, J Tinnert, L Wennersten and to four anonymous one is concerned with effects mediated by variation among reviewers for discussion and comments on the manuscript. This work was individuals in the capacity to express plasticity and flexibility, or funded by The Swedish Research Council and Linnaeus University. with effects driven by greater interindividual phenotypic variation resulting from induced responses (in which case there need be no genetic variation in plasticity). Agrawal AA (2001). Phenotypic plasticity in the interactions and evolution of species.  To put predictions to empirical tests, we must be able to quantify Science 294: 321–326. and compare the nature and magnitude of plasticity among Ahnesjö J, Forsman A (2006). Differential habitat selection by pygmy grasshopper color individuals, populations and species. In the wait of estimates of morphs; interactive effects of temperature and predator avoidance. Evol Ecol 20: 235–257. whole organism plasticity, multiple phenotypic dimensions can be Araya-Ajoy YG, Dingemanse NJ (2014). Characterizing behavioural ‘characters’: an examined, modelled and compared using multivariate statistical evolutionary framework. Proc R Soc B 281: 20132645. Arnold SJ, Bennett AF (1988). Behavioral variation in natural populations. V. Morphological analysis or by using composite measures of plasticity based on correlates of locomotion in the garter snake Thamnophis radix. Biol J Linn Soc 34: averages across traits or dimension reducing techniques. 175–190. Heredity  Rethinking plasticity and its consequences A Forsman 283 Arnold SJ. (1988). Proceedings of the Second Interntaional Conference on Quantitative Ketterson ED, Nolan V Jr., Cawthorn MJ, Parker PG, Ziegenfus C (1996). Phenotypic Genetics. In: Weir BS, Goodman MM, Eisen EJ, Namkong G (eds). Sinauer Associates, engineering: using hormones to explore the mechanisms and functional bases of pp 619–636. phenotypic variation in nature. Ibis 138: 70–86. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD et al. (2003). The Krebs RA, Feder ME (1998). Experimental manipulation of the cost of thermal acclimation ecology of individuals: incidence and implications of individual specialization. Am Nat in Drosophila melanogaster. Biol J Linn Soc 63: 593–601. 161: 1–28. Kurashige NS, Callahan HS (2007). Evolution of active and passive forms of plasticity: Booth RE, Grime JP (2003). Effects of genetic impoverishment on plant community insights from artificially selected Arabidopsis. Evol Ecol Res 9: 1–11. diversity. J Ecol 91: 721–730. Leimar O (2009). Environmental and genetic cues in the evolution of phenotypic plasticity. Bradshaw AD (1965). Evolutionary significance of phenotypic plasticity in plants. Adv Evol Ecol 23: 125–135. Genet 13: 115–155. Leimar O, Hammerstein P, Van Dooren TJM (2006). A new perspective on Brommer JE (2013). Phenotypic plasticity of labile traits in the wild. Curr Zool 59: developmental plasticity and the principles of adaptive morph determination. Am Nat 485–505. 167: 367–376. Bruni NC, Young JP, Dengler NG (1996). Leaf developmental plasticity of Ranunculus Levins R (1968). Evolution in Changing Environments. Princeton University Press: flabellaris in response to terrestrial and submerged environments. Can J Bot 74: Princeton. 823–837. Lindell LE (1994). The evolution of vertebral number and body size in snakes. Funct Ecol Carroll SP, Corneli PS (1995). Divergence in male mating tactics between two populations 8: 708–719. of the soapberry bug: II. Genetic change and the evolution of a plastic reaction norm in a Lindell LE, Forsman A (1996). Density effects and snake predation: prey limitation and variable social environment. Behav Ecol 6: 46–56. reduced growth rate of adders at high density of conspecifics. Can J Zool 74: Chevin L-M, Gallet R, Gomulkiewicz R, Holt RD, Fellous S (2013). Phenotypic plasticity in 1000–1007. evolutionary rescue experiments. Philos Trans R Soc B Biol Sci 368: 20120089. Lindell LE, Forsman A, Merilä J (1993). Variation in number of ventral scales in snakes - Chevin L-M, Lande R, Mace GM (2010). Adaptation, plasticity and extinction in a changing effects on body size, growth-rate and survival in the adder, Vipera berus. J Zool 230: environment: towards a predictive theory. PLoS Biol 8: e1000357. 101–115. Chun YJ (2011). Phenotypic plasticity of introduced versus native purple loosestrife: Lynch M, Walsh B (1998). Genetics and Analysis of Quantitative Traits. Sinauer Associates, univariate and multivariate reaction norm approaches. Biol Invasions 13: 819–829. Inc.: Sunderland, MA. Colbourne JK, Herbert PDN, Taylor DJ (1997). Evolutionary origins of phenotypic diversity Meyers LA, Bull JJ (2002). Fighting change with change: adaptive variation in an in Daphnia. In: Givnish TJ, Systma KJ (eds). Molecular Evolution and Adaptive uncertain world. Trends Ecol Evol 17: 551–557. Radiation. Cambridge University Press: Cambridge, pp 163–188. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005). Ecological consequences Davidson AM, Jennions M, Nicotra AB (2011). Do invasive species show higher phenotypic of phenotypic plasticity. Trends Ecol Evol 20: 685–692. plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14: Mousseau TA, Fox CW (1998). The adaptive significance of maternal effects. Trends Ecol 419–431. Evol 13: 403–407. Day T, Bonduriansky R (2011). A unified approach to the evolutionary consequences of Naeem S, Bunker DE, Hector A, Loreau M, Perrings C (eds) (2009). Biodiversity, genetic and nongenetic inheritance. Am Nat 178: E18–E36. Ecosystem Functioning, and Human Wellbeing. An Ecological and Economic Perspec- Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010). Behavioural reaction norms: tive. Oxford University Press: Oxford, pp 356. animal personality meets individual plasticity. Trends Ecol Evol 25: 81–89. Newman SA, Müller GB (2000). Epigenetic mechanisms of character origination. J Exp Edelaar P, Siepielski AM, Clobert J (2008). Matching habitat choice causes directed Zool 288: 304–317. gene flow: a neglected dimension in evolution and ecology. Evolution 62: Nunes AL, Orizaola G, Laurila A, Rebelo R (2013). Rapid evolution of constitutive and 2462–2472. inducible defenses against an invasive predator. Ecology 95: 1520–1530. Feder ME (1999). Engineering candidate genes in studies of adaptation: the heat-shock Nussey DH, Wilson AJ, Brommer JE (2007). The evolutionary ecology of individual protein Hsp70 in Drosophila melanogaster. Am Nat 154: S55–S66. phenotypic plasticity in wild populations. J Evol Biol 20: 831–844. Forsman A (1995). Heating rates and body temperature variation in melanistic and zigzag Olson EC, Miller RL (1958). Morphological Integration. University of Chicago Press: Vipera berus: does colour make a difference? Ann Zool Fennici 32: 365–374. Chicago. Forsman A (1996a). Body size and net energy gain in gape-limited predators: a model. J Pfennig DW, McGee M (2010). Resource polyphenism increases species richness: a test of Herpetol 30: 307–319. the hypothesis. Philos Trans R Soc B Biol Sci 365: 577–591. Forsman A (1996b). An experimental test for food effects on head size allometry in Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010). juvenile snakes. Evolution 50: 2536–2542. Phenotypic plasticity’s impact on diversification and speciation. Trends Ecol Evol 25: Forsman A (2014). Effects of genotypic and phenotypic variation on establishment are 459–467. important for conservation, invasion and infection biology. Proc Natl Acad Sci USA 111: Piersma T, Drent J (2003). Phenotypic flexibility and the evolution of organismal design. 302–307. Trends Ecol Evol 18: 228–233. Forsman A, Ahnesjö J, Caesar S, Karlsson M (2008). A model of ecological and evolutionary Piersma T, van Gils JA (2011). The Flexible Phenotype: A Body-Centred Integration of consequences of color polymorphism. Ecology 89: 34–40. Ecology, Physiology, and Behaviour. Oxford University Press. Forsman A, Lindell E (1996). Resource dependent growth and body condition dynamics in Pigliucci M (1996). How organisms respond to environmental changes: from phenotypes to juvenile snakes: an experiment. Oecologia 108: 669–675. molecules (and vice versa). Trends Ecol Evol 11: 168–173. Forsman A, Lindell LE (1993). The advantage of a big head - swallowing performance in Pigliucci M (2001). Phenotypic Plasticity Beyond Nature and Nurture. The John Hopkins adders, Vipera berus. Funct Ecol 7: 183–189. University Press: Baltimore. Forsman A, Ringblom K, Civantos E, Ahnesjö J (2002). Coevolution of color pattern and Pigliucci M (2005). Evolution of phenotypic plasticity: where are we going now? Trends thermoregulatory behavior in polymorphic pygmy grasshoppers Tetrix undulata. Evolu- Ecol Evol 20: 481–486. tion 56: 349–360. Pigliucci M (2010). Phenotypic plasticity. In: Pigliucci M, Müller GB (eds). Evolution - The Fox CW, Reed DH (2010). Inbreeding depression increases with environmental stress: an Extended Synthesis. Massachusetts Institute of Technology: Massachusetts, pp experimental study and meta-analysis. Evolution 65: 246–258. 355–378. Frank SA (2011). Natural selection. II. Developmental variability and evolutionary rate. Pigliucci M, Cammell K, Schmitt J (1999). Evolution of phenotypic plasticity a J Evol Biol 24: 2310–2320. comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana. Frank SA, Slatkin M (1990). Evolution in a variable environment. Am Nat 136: J Evol Biol 12: 779–791. 244–260. Pigliucci M, Pollard H, Cruzan MB (2003). Comparative studies of evolutionary responses Frankham R, Ballou JD, Briscoe DA (2010). Introduction to Conservation Genetics, to light environments in Arabidopsis. Am Nat 161: 68–82. 2nd edn. Cambridge University Press: Cambridge, UK. Pigliucci M, Preston K (2004). Phenotypic Integration: Studying the Ecology and Evolution Fristrup KM (2001). A history of character concepts in evolutionary biology. In: Wagner GP of Complex Phenotypes. Oxford University Press: Oxford. (ed). The Character Concept in Evolutionary Biology. Academic Press: San Diego, Pollard H, Cruzan M, Pigliucci M (2001). Comparative studies of reaction pp 13–35. norms in Arabidopsis. I. Evolution of response to daylength. Evol Ecol Res 3: Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007). Adaptive versus non-adaptive 129–155. phenotypic plasticity and the potential for contemporary adaptation in new environ- Price TD, Qvarnström A, Irwin DE (2003). The role of phenotypic plasticity in driving ments. Funct Ecol 21: 394–407. genetic evolution. Proc R Soc B 270: 1433–1440. Gray SM, McKinnon JS (2007). Linking color polymorphism maintenance and speciation. Reed TE, Waples RS, Schindler DE, Hard JJ, Kinnison MT (2010). Phenotypic plasticity Trends Ecol Evol 22: 71–79. and population viability: the importance of environmental predictability. Proc R Soc B Huey RB, Kingsolver JG (1989). Evolution of thermal sensitivity of ectotherm performance. 277: 3391–3400. Trends Ecol Evol 4: 131–135. Roff DA (1997). Evolutionary Quantitative Genetics. Chapman & Hall: New York. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008). Ecological Roff DA, Fairbairn DJ (2007). The evolution and genetics of migration in insects. consequences of genetic diversity. Ecol Lett 11: 609–623. Bioscience 57: 155–164. Jablonka E, Lamb MJ (2006). Evolution in Four Dimensions. MIT Press: Cambridge, MA. Saito N, Ishihara S, Kaneko K (2013). Baldwin effect under multipeaked fitness Karpestam E, Wennersten L, Forsman A (2012). Matching habitat choice by experimentally landscapes: phenotypic fluctuation accelerates evolutionary rate. Physical Review E 87: mismatched phenotypes. Evol Ecol 26: 893–907. 052701. Kendall BE, Fox GA (2002). Demographic factors and genetic variation influence Sarà M (1996). A “sensitive” cell system. Its role in a new evolutionary paradigm. Riv Biol population persistence under environmental change. Conserv Biol 16: 109–116. 89: 139–156. Heredity  Rethinking plasticity and its consequences A Forsman 284 Scheiner SM (2006). Genotype-environment interactions and evolution. In: Fox CW, Wolf Thaler JS, Karban R (1997). A phylogenetic reconstruction of constitutive and induced CM (eds). Evolutionary Genetics: Concepts and Case Studies. Oxford University Press: resistance in Gossypium. Am Nat 149: 1139–1146. New York, pp 326–338. Tonsor SJ, Elnaccash TW, Scheiner SM (2013). Developmental instability is genetically Scheiner SM, DeWitt TJ (2004). Future research directions. In: DeWitt TJ, Scheiner SM correlated with phenotypic plasticity, constraining heritability, and fitness. Evolution 67: (eds). Phenotypic Plasticity: Funcitonal and Conceptual Approaches. Oxford University 2923–2935. Press: New York, pp 201–207. Tuomainen U, Candolin U (2011). Behavioural responses to human-induced Schlichting CD (2003). Origins of differentiation via phenotypic plasticity. Evol Dev 5: environmental change. Biol Rev 86: 640–657. 98–105. Valladares F, Gianoli E, Gómez JM (2007). Ecological limits to plant phenotypic plasticity. Schlichting CD, Pigliucci M (1998). Phenotypic Evolution: A Reaction Norm Perspective. New Phytologist 176: 749–763. Sinauer Associates: Sunderland, MA, USA. Vedder O, Bouwhuis S, Sheldon BC (2013). Quantitative assessment of the importance of Schwander T, Leimar O (2011). Genes as leaders and followers in evolution. Trends Ecol phenotypic plasticity in adaptation to climate change in wild bird populations. PLoS Biol Evol 26: 143–151. 11: e1001605. Shine R (1991). Australian Snakes. A Natural History. Reed: Sydney. Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C et al. (2012). The return of Shine R (2000). Vertebral numbers in male and female snakes: the roles of natural, sexual the variance: intraspecific variability in community ecology. Trends Ecol Evol 27: and fecundity selection. J Evol Biol 13: 455–465. 244–252. Shuster SM (2010). Alternative mating strategies. In: Westneat DF, Fox CW (eds). Wennersten L, Forsman A (2012). Population-level consequences of polymorphism, Evolutionary Behavioral Ecology. Oxford Univeristy Press: New York, pp 434–450. plasticity and randomized phenotype switching: a review of predictions. Biol Rev 87: Sinervo B, Huey R (1990). Allometric engineering: an experimental test of the causes of 756–767. interpopulational differences in performance. Science 248: 1106–1109. West-Eberhard MJ (2003). Developmental Plasticity and Evolution. Oxford University Press: Snell-Rood EC (2013). An overview of the evolutionary causes and consequences of Oxford. behavioural plasticity. Anim Behav 85: 1004–1011. Whitlock R, Grime JP, Booth R, Burke T (2007). The role of genotypic diversity in Stamps J, Groothuis TGG (2010). The development of animal personality: relevance, determining grassland community structure under constant environmental conditions. concepts and perspectives. Biol Rev 85: 301–325. J Ecol 95: 895–907. Stearns SJ (1989). The evolutionary significance of phenotypic plasticity - phenotypic Whitman DW, Agrawal AA (2009). What is phenotypic plasticity and why is it important? sources of variation among organisms can be described by developmental switches and In: Whitman DW, Ananthakrishnan TN (eds). Phenotypic Plasticity of Insects: Mechanisms and Consequences. Science Publishers: Enfield, pp 1–63. reaction norms. Bioscience 39: 436–445. Wund MA (2012). Assessing the impacts of phenotypic plasticity on evolution. Integr Comp Stevenson RD (1985a). Body size and limits to the daily range of body temperature in Biol 52: 5–15. terrestrial ectotherms. Am Nat 125: 102–117. Zera AJ (2003). The endocrine regulation of wing polymorphism in insects: state of the art, Stevenson RD (1985b). The relative importance of behavioral and physiological recent surprises, and future directions. Integr Comp Biol 43: 607–616. adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126: 362–386. Sultan SE (2000). Phenotypic plasticity for plant development, function and life history. Trends in Plant Science 5: 537–542. This work is licensed under a Creative Commons Sultan SE (2003). Phenotypic plasticity in plants: a case study in ecological development. Attribution-NonCommercial-ShareAlike 3.0 Unported Evol Dev 5: 25–33. Sultan SE (2004). Promising directions in plant phenotypic plasticity. Persp Plant Eco Evol License. The images or other third party material in this article are Syst 6: 227–233. included in the article’s Creative Commons license, unless indicated Sánchez Alvarado A, Yamanaka S (2014). Rethinking differentiation: stem cells, regenera- otherwise in the credit line; if the material is not included under the tion, and plasticity. Cell 157: 110–119. te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M et al. (2011). Creative Commons license, users will need to obtain permission from The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109: the license holder to reproduce the material. To view a copy of this 19–45. license, visit http://creativecommons.org/licenses/by-nc-sa/3.0/ Heredity