The question of whether plasticity is adaptive is dependent upon the environment in which it is expressed. For the purposes of this article, we are concerned with two environments: the current environment and a new one that the population must adapt to. A new environment can be defined by a change in the current environment or by the invasion of a new habitat. By definition any plasticity that allows individuals to have higher fitness in the new environment than it would were it not plastic will be beneficial. However, this does not mean that the reaction norm for a given trait was necessarily shaped by natural selection (i.e. be an adaptation in itself; Gotthard & Nylin 1995). Thus, it is necessary to specify the impact different kinds of plasticity might have in the face of directional selection. Below, we explore these ideas by considering general scenarios where a newly established population experiences selection for a new adaptive peak (following the framework of Price et al. 2003).
Adaptive reaction norms: perfect vs incomplete responses
A second step of adaptation to new environments via adaptive plasticity can be the conversion of non-heritable environmentally induced variation to heritable variation, a scenario that remains controversial despite theoretical and empirical arguments dating back over a century (e.g. Baldwin 1896; Waddington 1942, 1952, 1953, 1956, 1959; Schmalhausen 1949). The process by which non-heritable environmentally induced variation leads to adaptive heritable variation is often referred to as the Baldwin Effect or more commonly as genetic assimilation (e.g. Waddington 1942, 1952, 1953; Simpson 1953; Robinson & Dukas 1999; Pigliucci & Murren 2003; Price et al. 2003; West-Eberhard 2003; Schlichting 2004). Specifically, genetic assimilation is when traits that were originally environmentally induced become (by the process of directional selection) genetically determined and canalized (a loss of plasticity or a flat reaction norm). West-Eberhard (2003) advocates a less restrictive term genetic accommodation, which does not necessarily lead to a loss in plasticity. This process can be illustrated with a hypothetical example following West-Eberhard's framework with her general terminology in italics and parentheses as follows: (i) Assume a population of a brightly coloured fish that typically occurs in low predation lakes. (ii) Within the population there is genetic variation for predator-induced phenotypic plasticity in cryptic colouration (an environmentally induced phenotypic variant as opposed to one determined by a mutation – the origin of the trait). (iii) A predator colonizes the lake and many individuals exhibit adaptive plasticity for cryptic colouration and other behaviours that collectively allow for a higher probability of survival compared to individuals that lack plasticity (phenotypic accommodation by individual phenotypes). (iv) Within this selective environment, only those individuals capable of producing the plastic response survive and reproduce (the recurrence of the environmental stimulus leads to a subpopulation of individuals that always express the induced phenotype and facilitates its spread in the population). (v) Directional selection favouring the most cryptic individuals in the population leads to allelic substitutions in the regulatory pathway that controls colour patterns and the loss of individuals capable of expressing bright colour (genetic accommodation). (vi) The establishment of a population that is genetically differentiated from its ancestral state and either constitutively produces cryptic colouration (i.e. canalization) or has become more plastic in response to the presence of the predator (i.e. the slope of the reaction norm has becomes steeper). Waddington's (1953) experiments on the genetic assimilation of the loss of cross-veins in Drosophila wings in response to heat shock followed an analogous scenario in the laboratory. West-Eberhard (2003) has championed this view as a potentially common or perhaps the predominant way by which adaptive evolution occurs (see also Pigliucci & Murren 2003). A key to this argument, and to Waddington's results, is that while the plasticity is environmentally induced, there must still be underlying genetic variation in inducibility and expression (see also de Jong 2005). It is this underlying variation that provides the basis for adaptation. Indeed, while a variety of models confirm that adaptive plasticity may facilitate adaptive evolution (e.g. Hinton & Nowlan 1987; Behera & Nanjundiah 2004; Ancel 1999), others have shown how plasticity slows the rate of evolution (e.g. Behera & Nanjundiah 1995; Ancel 2000, Huey, Hertz & Sinervo 2003). Below we contrast when adaptive plasticity is likely to slow or speed up the rate of adaptation.
The rate of adaptation to new environments is likely to differ depending on how close the plastic phenotype is to the optimum favoured in the new environment (Price et al. 2003). When adaptive plasticity produces a near perfect match with the optimal phenotype in the new environment (the all purpose genotype in Fig. 1a), the population should experience stabilizing selection with no subsequent genetic differentiation between populations unless there is a substantial fitness cost to plasticity (e.g. Price et al. 2003). In other words, adaptive plasticity should slow or constrain adaptive genetic differentiation between populations. The introduced C4 grass Pennisetum setaceum (fountaingrass) in Hawaii may be a case where adaptive plasticity is so good it has prevented adaptive evolution. Fountaingrass is native to North Africa and the Middle East and was introduced as an ornamental into Hawaii over 100 years ago, where it spread rapidly in arid zones (Wagner, Herbst & Sohmer 1990). On the island of Hawaii, fountaingrass colonizes disturbed sites and can become dominant within communities ranging from sea level to almost 3000-m altitude (Wagner et al. 1990). Williams, Mack & Black (1995) investigated whether populations from coastal dry grasslands, mid-altitude shrubland and subalpine dry forest sites were genetically differentiated from each other. These sites experience large differences in the seasonal pattern of precipitation and temperature declines markedly with increasing altitude such that coastal sites never experience frost, whereas winter night time frost is common at the subalpine sites (Williams et al. 1995). Individuals from these sites exhibit dramatic differences in morphology, physiology and reproductive strategies that result in locally adaptive, and phenotypically distinct populations (Williams et al. 1995). However, despite very different phenotypes and selective environments, reciprocal transplant experiments reveal little genetic differentiation for most physiological and morphological characters between these populations (Williams et al. 1995). One interpretation of these results is that adaptive plasticity results in such a good match with the environment when there is no opportunity for directional selection to act and hence no evolution. Alternatively, because fountaingrass may have been founded by a small population, there may not be sufficient genetic variation in these populations for selection to act on (Williams et al. 1995). However, a non-significant trend for resident populations at each site to have higher fitness, and for some local adaptation of traits between populations, suggests the potential for genetic differentiation exists (Williams et al. 1995). Other examples of adaptive plasticity producing near perfect responses to different environments and constraining genetic differentiation have been documented in a variety of systems (e.g. Dudley & Schmitt 1996; Mittelbach, Osenberg & Wainwright 1999; Lorenzon, Clobert & Massot 2001).
Adaptive plasticity may also result in an incomplete response relative to the new optimum, meaning that the change in the mean trait value is in the same direction favoured by selection in the new environment, but below the new adaptive peak (Fig. 1a). In such cases, the new population will be subjected to directional selection on extreme phenotypes and the potential for adaptation should be facilitated (reviewed in Price et al. 2003). Because environments are typically heterogeneous in space and time, incomplete adaptive plasticity is likely to be the most common form of adaptive plasticity. The evolution of offspring size in Trinidadian guppies (Poecilia reticulata) is an example in which incomplete adaptive plasticity may have served as a bridge to evolved adaptation. Guppies are often found in either downstream sites where they co-occur with many predators or in headwater streams where these predators are excluded by waterfalls and rapids (Endler 1978). These low predation headwater streams also tend to have lower light levels and lower primary productivity than high predation streams, which in combination with higher densities of guppies results in greater food limitation (Reznick, Butler & Rodd 2001). Selection is thought to favour larger offspring under such competitive conditions (Bashey 2006). Guppies from low predation environments produce fewer and larger offspring than their counterparts from high predation environments (Reznick, Rodd & Cardenas 1996; Bashey 2006). While these size differences can be shown to have a genetic basis (Reznick 1982; Reznick & Bryga 1996), there is also considerable plasticity in offspring size; female guppies that are reared on low food rations or that experience variation in food availability produce offspring that are 15%–20% larger than those that are kept on constant, high food rations (Reznick & Yang 1993). Thus, the plastic response in offspring size is in the same direction favoured by selection in the low predation environments. Larger offspring in response to lower food availability appear adaptive, because larger offspring have a competitive advantage when food availability is low but not when it is high (Bashey 2006). Genetic analyses suggest that low predation populations have independently originated from downstream high predation regions (e.g. Crispo et al. 2006). Such a repeated pattern of colonization means that guppies would regularly experience a reduction in food availability as they move upstream and hence experience selection for increased offspring size. Their ability to produce larger offspring in response to low food availability represents an adaptive plastic response that would increase the probability that they could successfully invade these environments, while their genetic capacity to produce larger offspring is likely to represent an adaptation that follows such invasions. Significant genetic changes in offspring size were recorded after 11 years (approximately 16 generations) after transplanting guppies from a high to a low predation environment (Reznick & Bryga 1987; Reznick, Bryga & Endler 1990; Reznick et al. 1997). Thus, plasticity in offspring size does not appear to retard adaptive evolution in guppies, and may even facilitate adaptation to low predation environments, since it will result in females producing larger offspring as soon as they become established in low predation environments, more than a decade before there is detectable evolution in the trait. Other examples of incomplete adaptive plastic responses with respect to the optimum phenotype known to evolve have been documented in various systems (e.g. Day, Pritchard & Schluter 1994; Chapman, Frieston & Shinn 2000; Trussell 2000; Losos et al. 2000; Donohue et al. 2000; Yeh & Price 2004).
Non-adaptive reaction norms: environmental heterogeneity and stress
In contrast to new environments that are reasonably similar to native or ancestral ones, new environments that fall outside the range of conditions typically experienced by populations are often studied from the perspective of ‘environmental stress’ (e.g. Bradshaw & Hardwick 1989; Bijlsma & Loeschcke 1997; Hoffman & Parsons 1997; Badyaev 2005). Here we define stress as new environments that lie outside the range of preferred conditions and impose a challenge to an organism's ability to maintain homeostasis and proper function. New environments that are stressful will thus pose a twofold challenge to newly established populations: (i) maintaining homeostasis and proper development, and (ii) responding to strong directional selection (e.g. Waddington 1941; Bradshaw & Hardwick 1989). The solution to the first challenge lies in the ability of organisms to buffer themselves against these stresses so that proper development and function can still occur (e.g. Waddington 1953; Scharloo 1991), whereas the solution to the second challenge is dependent on the relationship between stress-induced phenotypic and genetic variation, and the prevailing selection pressure (e.g. Rutherford & Lindquist 1998; Badyaev 2005). In such cases, canalization (i.e. a lack of plasticity) for the most basic physiological and developmental processes to properly function is the best hope for increasing the likelihood of persistence in the new environment. Stressful environments thus illustrate the challenge or trade-off of having a genotype capable of producing the same target (canalized) phenotype under different environments vs a genotype having the ability to produce many potentially adaptive phenotypes in different environments (i.e. plasticity).
Non-adaptive plasticity in response to stress may reflect a fundamental breakdown during development or disruption of physiological function because of changes in temperature, pH or moisture that fall outside of the range historically experienced. By non-adaptive we mean that compared to the ancestral phenotype, the environmentally induced phenotype in the new environment has on average reduced fitness or is further away from the new adaptive peak (Fig. 1B). This type of non-adaptive plasticity represents a fundamentally different kind of environmentally induced effect compared to situations where past selection on the reaction norm allows for adaptive plasticity, and better matching of the phenotype and the environment. It is perhaps the most common form of plasticity to environmental heterogeneity, arising as a ‘passive’ consequence to environmental stress (e.g. Dorn, Pyle & Schmitt 2000; Grether 2005; van Kleunen & Fisher 2005).
In such cases, the slope of the reaction norm is such that the optimal phenotype in the new environment is not produced and the plastic response is usually a non-adaptive shift in the mean trait value away from the new optimum (Fig. 1b). Here a lack of plasticity or canalized response, that allows organisms to produce the same phenotype regardless of environment results in the best strategy (Fig. 1b). For example, plants may fail to grow to an optimal height and produce few seeds when occupying a microenvironment that is lacking moisture and/or essential minerals (e.g. van Kleunen & Fisher 2005). Grether (2005) argues that this kind of non-adaptive plasticity is likely to underlie a form of cryptic evolution because it results in strong directional selection that makes populations in different environments similar to one another as is observed under ‘countergradient variation’ (e.g. Conover & Schultz 1995; Carroll et al. 2001; Trussell & Etter 2001). Grether (2005) refers to this process as ‘genetic compensation’ to distinguish it from genetic assimilation because selection results in evolutionary changes that serve to re-establish the phenotype because the same optima are favoured in both the new and the ancestral environments.
The anadromous Sockeye salmon and non-anadromous lake-bound Kokanee are genetically distinct forms of Pacific salmon (Oncorhynchus nerka) that provide a good example of how environmental stress acting through a limiting resource results initially in non-adaptive plasticity and ultimately in cryptic adaptive evolution (Craig & Foote 2001; Craig, Foote & Wood 2005). Kokanee populations appear to have evolved repeatedly from anadromous Sockeye individuals that failed to return to the ocean (called ‘residuals’). Kokanee therefore tend to be more closely related to Sockeye inhabiting the same lakes for breeding, than to (phenotypically similar) Kokanee in other lakes (e.g. Foote, Wood & Withler 1989; Taylor, Foote & Wood 1996; Wood & Foote 1996). Both Sockeye and Kokanee turn from silver to bright red when they mature and move into streams to spawn, whereas residual Sockeye are distinguished by their olive green skin at maturity (Craig & Foote 2001; Craig et al. 2005). The bright red colouration is produced through the acquisition of dietary carotenoids; however, despite Sockeye and Kokanee exhibiting identical red colouration, carotenoid availability is much lower in lakes than it is in the oceans (Craig & Foote 2001). By crossing Sockeye and Kokanee, and measuring their offspring under common environmental conditions, Craig & Foote (2001) found that Kokanee are three times more efficient in acquiring and depositing carotenoids in their flesh than Sockeye. In addition, mate choice trials revealed a strong preference in Sockeye for red colouration over green, suggesting that the evolution from green colouration (residuals) to red colouration (Kokanee) is driven by sexual selection (Craig & Foote 2001). These results argue for a compelling case of genetic differentiation via a series of events: (i) ancestral Sockeye colonize freshwater lakes via residuals, (ii) residuals initially fail to produce the desired phenotype due to resource limitation, and (iii) directional selection leads to the evolution of greater efficiency in the use of dietary carotenoids and the return of the ancestral or favoured phenotype. Grether (2005) reviews other examples of evolutionary change via a similar process.
Another perspective on non-adaptive plasticity and adaptive evolution considers the role stressful environments play in increasing the expression of genetic and phenotypic variance (e.g. Hoffmann & Parsons 1997; Hoffmann & Merilä 1999). In contrast to the previously discussed types of plasticity that act primarily on the mean value of a trait, stressful environments that fall far outside the range historically encountered can break down genetic buffering mechanisms, and in turn increase the variance associated with different traits (e.g. Rutherford 2000, 2003). This type of stress-induced plasticity is thought to reveal cryptic genetic variation which results in an increase in the genotypic and phenotypic variance that is ‘hidden’ or unexpressed under normal environmental conditions (e.g. Rutherford & Lindquist 1998; Rutherford 2000, 2003; Ruden et al. 2003; see also Schlichting 2004). In other words, under typical environmental conditions most individuals in a population will exhibit similar patterns of plasticity (low variance), whereas under stressful environments individuals diverge in their response (high variance). An important aspect of this perspective is that most of the stress induced variants are likely to be quickly eliminated by selection in the new stressful environment because they exhibit deleterious phenotypes. Indeed, studies that have used environmental stress to express cryptic genetic variation produce phenotypes that would be unlikely to survive and reproduce under most natural condition (Rutherford & Lindquist 1998; Queitsch, Sangster & Lindquist 2002). However, if by chance a small number of genotypes exhibit a beneficial plastic response that either allows a subset of individuals to persist long enough to survive and reproduce in the new environment for directional selection to act (see above) or is passed on via a maternal or epigenetic effect, adaptive evolution may occur (Rutherford 2000, 2003).
An often cited example documenting the interplay between stress, plasticity, and the potential for adaptive evolution via the increased expression of genetic and phenotypic variation are the heat shock proteins (HSPs), specifically Hsp90 (e.g. Rutherford & Lindquist 1998; Rutherford 2000, 2003; Queitsch et al. 2002). HSPs are families of enzymes and chaperones that are mobilized in large numbers by cells under temperature stress to assist in the correct folding of proteins (Rutherford 2000, 2003). In addition to its increased expression in response to elevated temperatures, Hsp90 also interacts in diverse signalling networks and is intimately involved in several developmental pathways (Rutherford & Lindquist 1998; Queitsch et al. 2002). These diverse functions place Hsp90 in the unique position of not only buffering organisms from external temperature stress, but also preventing the expression of genetic variants which accumulate but are not expressed, such that different genotypes reliably produce the same phenotype across a range of environments (Rutherford 2003). The buffering capacity of Hsp90 has been revealed in complimentary studies in Drosophila (Rutherford & Lindquist 1998) and Arabidopsis (Queitsch et al. 2002) which show that reduced Hsp90 function, whether due to mutation, chemical impairment or changes in temperature, results in significant increases in phenotypic variation due to the expression of previously cryptic genetic differences. While much of this cryptic variation would surely be deleterious under natural conditions, some of the Hsp90 controlled variation could possibly be advantageous under particular environmental conditions and result in an adaptive response (Queitsch et al. 2002). The ‘hopeful monsters’ associated with the release of cryptic genetic variation have been argued to provide a potential mechanism by which stressful environmental change may create the conditions for rapid adaptation through the release of novel variation that selection can act on (Rutherford & Lindquist 1998; Rutherford 2000, 2003; Queitsch et al. 2002). Badyaev (2005) reviews other examples where stress induced variation may have facilitated adaptive evolution.
The mosaic nature of plasticity and evolution in new environments
We have described how different types of plasticity in individual traits can lead to adaptive evolution. However, within any given individual, a new selective environment is likely to induce a variety of responses in different traits (e.g. Williams et al. 1995; Parsons & Robinson 2006). Thus, individuals are likely to be made up of both canalized traits that do not respond to novel environmental stimuli as well as traits that differ in the type of plasticity they exhibit (adaptive and non-adaptive), resulting in individuals that represent a mosaic of traits. What is the consequence of this mosaic nature in creating individual variation and its resultant importance to population persistence and adaptive evolution to new environments? To answer this question, we need to know more about: (i) whether suites of plastic and non-plastic traits respond independently or in an integrated manner to environmental change, and (ii) if and how the potential for adaptation is influenced by either of these scenarios. Only a few studies have been designed to consider such questions (e.g. Parsons & Robinson 2006), but in the case of the Soapberry bug (Jadera haematoloma) where reaction norms of seven traits were compared between recently ancestral and derived populations, the answer suggests a lack of integration. Floridian Soapberry bugs adopted an introduced plant as a food source in about 1960, a colonization event that caused selection on host-based performance reaction norms over the next tens of generations, and resulted in distinctive ‘host races’ (Carroll, Dingle & Klassen 1997; Carroll, Klassen & Dingle 1998). In the laboratory, bugs of each type were reared on seeds of each host to simultaneously compare reaction norms for beak length, body size, survivorship, development time, fecundity and other traits. Not unexpectedly, the response of certain traits was strongly correlated, such as larger-bodied individuals normally having longer beaks and larger eggs. In contrast however, the direction and magnitude of mean trait responses to being reared on alternate host were not closely correlated. For example, adults from the native host plant were substantially smaller-bodied when reared on the exotic host, but their beak length did not differ and was instead canalized. Most interestingly, in the reciprocal comparison with the derived race, that canalization is lost, and body and beak values responded with similar diminution when rearing was on the native host (Carroll et al. 1997). Thus, even among these recently diverged host races, the patterns of plastic and canalized responses can vary for the same traits.
The mosaic nature of the responses is further illustrated when the reaction norms of different traits are examined. For example, reduced survivorship and development rate of the native-host race reared on the new host reveals the evolutionary path via which countergradient selection has had to overcome stress induced plasticity in order to return the traits in the derived population to their former (ancestral) values (e.g. Carroll et al. 1997). In contrast, in other traits, including beak length, the pattern of plasticity on the new host plant is adaptive and in the same direction favoured by selection, suggesting a facilitating role of plasticity in moving the population closer to a new adaptive peak (Carroll et al. 1997). Thus, new maladapted and adaptive reaction norms may simultaneously be generated as a pleiotropic effect, but in other traits (e.g. egg size) the slope and magnitude of environmental effects may also remain the same.
The differentiation between Soapberry bug host races is substantial, and adaptive evolution was likely facilitated by the presence of an abundant new resource and the absence of competitors which permitted unfettered evolutionary ‘experimentation’ in a growing population (Reznick & Ghalambor 2001). Yet the complex mosaic of interacting plastic and non-plastic traits in response to directional selection that has produced the derived race shows that the bugs are altered far beyond what a superficial assessment of current phenotypic differences would suggest, given that some of the original values are now re-established. These results also suggest that adaptive plasticity in at least some traits may play an important role in population persistence to new environments and allowing time for directional selection to act on other traits that exhibit non-adaptive plasticity or are canalized. Such a perspective is consistent with long held ideas that adaptive plasticity in behaviour may help in population persistence to new environments and in turn facilitate evolutionary divergence in morphological or physiological traits (e.g. Losos, Schoener & Spiller 2004, but see Huey et al. 2003). Other currently diversifying populations provide an opportunity to examine the levels of genetic divergence, integrated plastic responses, and the interaction of relative degrees of plasticity and intensities of selection (Parsons & Robinson 2006; S.P. Carroll & C.W. Fox, unpublished).