Adaptive and nonadaptive plasticity in changing environments: Implications for sexual species with different life history strategies.

Drawing the line: Linear or non-linear reaction norms in response to adult acclimation on lower thermal limits

Adaptation to heterogeneous environments can occur via phenotypic plasticity, but how often this occurs is unknown. Reciprocal transplant studies provide a rich dataset to address this issue in plant populations because they allow for a determination of the prevalence of plastic versus canalized responses. From 31 reciprocal transplant studies, we quantified the frequency of five possible evolutionary patterns: (1) canalized response–no differentiation: no plasticity, the mean phenotypes of the populations are not different; (2) canalized response–population differentiation: no plasticity, the mean phenotypes of the populations are different; (3) perfect adaptive plasticity: plastic responses with similar reaction norms between populations; (4) adaptive plasticity: plastic responses with parallel, but not congruent reaction norms between populations; and (5) nonadaptive plasticity: plastic responses with differences in the slope of the reaction norms. The analysis included 362 records: 50.8% life-history traits, 43.6% morphological traits, and 5.5% physiological traits. Across all traits, 52% of the trait records were not plastic, and either showed no difference in means across sites (17%) or differed among sites (83%). Among the 48% of trait records that showed some sort of plasticity, 49.4% showed perfect adaptive plasticity, 19.5% adaptive plasticity, and 31% nonadaptive plasticity. These results suggest that canalized responses are more common than adaptive plasticity as an evolutionary response to environmental heterogeneity.

We present a general quantitative genetic model for the evolution of reaction norms. This model goes beyond previous models by simultaneously permitting any shaped reaction norm and allowing for the imposition of genetic constraints. Earlier models are shown to be special cases of our general model; we discuss in detail models involving just two macroenvironments, linear reaction norms, and quadratic reaction norms. The model predicts that, for the case of a temporally varying environment, a population will converge on (1) the genotype with the maximum mean geometric fitness over all environments, (2) a linear reaction norm whose slope is proportional to the covariance between the environment of development and the environment of selection, and (3) a linear reaction norm even if nonlinear reaction norms are possible. An examination of experimental studies finds some limited support for these predictions. We discuss the limitations of our model and the need for more realistic gametic models and additional data on the genetic and developmental bases of plasticity.

Genetic assimilation emerges from selection on phenotypic plasticity. Yet, commonly used quantitative genetics models of linear reaction norms considering intercept and slope as traits do not mimic the full process of genetic assimilation. We argue that intercept-slope reaction norm models are insufficient representations of genetic effects on linear reaction norms and that considering reaction norm intercept as a trait is unfortunate because the definition of this trait relates to a specific environmental value (zero) and confounds genetic effects on reaction norm elevation with genetic effects on environmental perception. Instead, we suggest a model with three traits representing genetic effects that, respectively, (i) are independent of the environment, (ii) alter the sensitivity of the phenotype to the environment and (iii) determine how the organism perceives the environment. The model predicts that, given sufficient additive genetic variation in environmental perception, the environmental value at which reaction norms tend to cross will respond rapidly to selection after an abrupt environmental change, and eventually becomes equal to the new mean environment. This readjustment of the zone of canalization becomes completed without changes in genetic correlations, genetic drift or imposing any fitness costs of maintaining plasticity. The asymptotic evolutionary outcome of this three-trait linear reaction norm generally entails a lower degree of phenotypic plasticity than the two-trait model, and maximum expected fitness does not occur at the mean trait values in the population.

Adaptive phenotypic plasticity may improve the response of individuals when faced with new environmental conditions. Typically, empirical evidence for plasticity is based on phenotypic reaction norms obtained in reciprocal transplant experiments. In such experiments, individuals from their native environment are transplanted into a different environment, and a number of trait values, potentially implicated in individuals' response to the new environment, are measured. However, the interpretations of reaction norms may differ depending on the nature of the assessed traits, which may not be known beforehand. For example, for traits that contribute to local adaptation, adaptive plasticity implies nonzero slopes of reaction norms. By contrast, for traits that are correlated to fitness, high tolerance to different environments (possibly due to adaptive plasticity in traits that contribute to adaptation) may, instead, result in flat reaction norms. Here we investigate reaction norms for adaptive versus fitness-correlated traits and how they may affect the conclusions regarding the contribution of plasticity. To this end, we first simulate range expansion along an environmental gradient where plasticity evolves to different values locally and then perform reciprocal transplant experiments in silico. We show that reaction norms alone cannot inform us whether the assessed trait exhibits locally adaptive, maladaptive, neutral, or no plasticity, without any additional knowledge of the traits assessed and species' biology. We use the insights from the model to analyse and interpret empirical data from reciprocal transplant experiments involving the marine isopod Idotea balthica sampled from two geographical locations with different salinities, concluding that the low-salinity population likely has reduced adaptive plasticity relative to the high-salinity population. Overall, we conclude that, when interpreting results from reciprocal transplant experiments, it is necessary to consider whether traits assessed are locally adaptive with respect to the environmental variable accounted for in the experiments or correlated to fitness.

Evidence supporting an association between phenotypic plasticity and invasiveness across a range of plant taxa is based primarily on comparisons between invasive species and native species whose potential invasiveness is typically unknown. Comparison of invasive and non-invasive exotic species would provide a better test of whether plasticity promotes invasion. Such comparisons should distinguish between adaptive and non-adaptive plasticity because they have different consequences for invasiveness. Adaptive plasticity is expected to promote the invasion of multiple habitats, but non-adaptive plasticity may reflect specialization for invading more favorable habitats only. We grew four invasive and four non-invasive species of the Commelinaceae with and without competitors and compared their putatively adaptive plasticity of three traits related to competitive ability and non-adaptive plasticity in performance. The invasive species grew significantly more than the non-invasive species only in the non-competitive environment. The invasive species had greater plasticity of performance (total biomass) in response to competition than non-invasives, but there was no consistent difference in the plasticities of the traits related to competitive ability. These results are consistent with specialization of these invasive taxa for invading the more productive non-competitive environment rather than a superior ability to invade both competitive and non-competitive environments. A comprehensive understanding of the relationship between plasticity and invasiveness will require many more comparisons of the plasticity of invasive and non-invasive taxa in a range of traits in response to a variety of environments.

Several studies have emphasized that inbreeding depression (ID) is enhanced under stressful conditions. Additionally, one might imagine a loss of adaptively plastic responses which may further contribute to a reduction in fitness under environmental stress. Here, we quantified ID in inbred families of the cyclical parthenogen Daphnia magna in the absence and presence of fish predation risk. We test whether predator stress affects the degree of ID and if inbred families have a reduced capacity to respond to predator stress by adaptive phenotypic plasticity. We obtained two inbred families through clonal selfing within clones isolated from a fish pond. After mild purging under standardized conditions, we compared life history traits and adaptive plasticity between inbred and outbred lineages (directly hatched from the natural dormant egg bank of the same pond). Initial purging of lineages under standardized conditions differed among inbred families and exceeded that in outbreds. The least purged inbred family exhibited strong ID for most life history traits. Predator-induced stress hardly affected the severity of ID, but the degree to which the capacity for adaptive phenotypic plasticity was retained varied strongly among the inbred families. The least purged family overall lacked the capacity for adaptive phenotypic plasticity, whereas the family that suffered only mild purging exhibited a potential for adaptive plasticity that was comparable to the outbred population. We thus found that inbred offspring may retain the capacity to respond to the presence of fish by adaptive phenotypic plasticity, but this strongly depends on the parental clone engaging in selfing.

Adaptive phenotypic plasticity evolves in response to the contrasting selection pressures that arise when organisms face environmental heterogeneity. Despite its importance for understanding how organisms successfully cope with environmental change, adaptive plasticity is often assumed but rarely demonstrated. We study here the adaptive nature of the extreme seasonal within-individual floral polyphenism exhibited by the crucifer Moricandia arvensis, a Mediterranean species that produces two different types of flowers depending on the season of the year. During spring, this species has large, cross-shaped, lilac flowers, while during summer, it develops small, rounded, white flowers. Although floral polyphenism was associated with increased plant fitness, selection moved floral traits away from their local optimum values during the harsh summer. This result strongly suggests that floral polyphenism is not adaptive in M. arvensis. The main factor selecting against floral polyphenism was pollinators, as they select for the same floral morph in all environments. Despite not being adaptive, floral polyphenism occurs throughout the entire distribution range of M. arvensis and has probably been present since the origin of the species. To solve this paradox, we explored the factors causing floral polyphenism, finding that floral polyphenism was triggered by summer flowering. Summer flowering was beneficial because it led to extra seed production and was favored by adaptive plasticity in leaf functional traits. Taken together, our study reveals a complex scenario in which nonadaptive floral polyphenism has been indirectly maintained over M. arvensis evolutionary history by selection operating to favor summer flowering. Our study provides thus strong evidence that nonadaptive plasticity may evolve as a byproduct of colonizing stressful environments.

The 21st century will be the century of biology, and evolutionary biology will be the linchpin. Yes, this is a bold statement, but it is certainly in keeping with Dobzhansky's famous dictum about evolution. Dobzhansky was one of the major architects of the Modern Synthesis. This book by Schlichting and Pigliucci (SP the Final Synthesis is just gathering steam. Note that these dates are just rough guides and not meant to imply that significant work did not occur outside those periods. What is critical is that within these periods the relevant disciplines all become focussed on the same research program. We are now in the midst of this final joining of biological disciplines. This joining, if history is a guide, will take the next couple of decades. This joining will be driven from the evolutionary side. It is the evolutionary side within which the disciplines are linked by a synthetic theory. The molecular side is primarily linked by a shared set of techniques and a viewpoint that centers all questions ultimately on DNA sequences. Because the evolution side is much more theory driven, that is where synthetic concepts tend to arise. This book by S&P is an excellent example of such theorydriven synthesis. Also, if truth be told, as a whole evolutionary biologists tend to have a larger perspective than those in many other biological disciplines. Looking back on the Modern Synthesis is useful for the task ahead (Mayr and Provine, 1980). In particular, if we learn anything from that episode in our history, we

Control of Phenotypic Plasticity Via Regulatory Genes

Fluctuating environmental conditions are ubiquitous in natural systems, and populations have evolved various strategies to cope with such fluctuations. The particular mechanisms that evolve profoundly influence subsequent evolutionary dynamics. One such mechanism is phenotypic plasticity, which is the ability of a single genotype to produce alternate phenotypes in an environmentally dependent context. Here, we use digital organisms (self-replicating computer programs) to investigate how adaptive phenotypic plasticity alters evolutionary dynamics and influences evolutionary outcomes in cyclically changing environments. Specifically, we examined the evolutionary histories of both plastic populations and non-plastic populations to ask: (1) Does adaptive plasticity promote or constrain evolutionary change? (2) Are plastic populations better able to evolve and then maintain novel traits? And (3), how does adaptive plasticity affect the potential for maladaptive alleles to accumulate in evolving genomes? We find that populations with adaptive phenotypic plasticity undergo less evolutionary change than non-plastic populations, which must rely on genetic variation from de novo mutations to continuously readapt to environmental fluctuations. Indeed, the non-plastic populations undergo more frequent selective sweeps and accumulate many more genetic changes. We find that the repeated selective sweeps in non-plastic populations drive the loss of beneficial traits and accumulation of maladaptive alleles, whereas phenotypic plasticity can stabilize populations against environmental fluctuations. This stabilization allows plastic populations to more easily retain novel adaptive traits than their non-plastic counterparts. In general, the evolution of adaptive phenotypic plasticity shifted evolutionary dynamics to be more similar to that of populations evolving in a static environment than to non-plastic populations evolving in an identical fluctuating environment. All natural environments subject populations to some form of change; our findings suggest that the stabilizing effect of phenotypic plasticity plays an important role in subsequent adaptive evolution.

Trade-off between resource allocation and acquisition in anadromous adult male Atlantic salmon (Salmo salar L.)

Theory predicts that adaptive plasticity in life history strategies should be favored in organisms with widely dispersed offspring because of the increased likelihood of encountering spatial and temporal environmental heterogeneity. Phenotypic plasticity is the ability of a genotype to produce different phenotypes across an environmental gradient (Bradshaw 1965; Schlichting and Pigliucci 1998; Debat and David 2001). Plasticity does not represent genetic change, although the form of change (the trait may increase in value, decrease, or remain the same) may be a product of selection. Phenotypic plasticity can be heuristically and graphically described as a norm of reaction, a linear or nonlinear function that expresses how the phenotypic value of a trait for a given genotype changes with the environment (Schmalhausen 1949; Schlichting and Pigliucci 1998).

Unpredictability during development of the optimum phenotype under future selection leads to a compromise reaction norm with a slope that is shallower than the slope of the optimum reaction norm. Unpredictability of selection can lead to an evolved curved reaction norm when genetic variation for curvature is available even if the optimum reaction norm is linear. This requires asymmetry in the frequency distribution of the habitats of selection; at small population size, stochasticity in the number of individuals per selection habitat is sufficient to generate such asymmetry. Unpredictability of selection in structured populations leads to local genetic differentiation of reaction norms. The mean habitat of a subpopulation is defined as the subpopulation's focal habitat. The evolved mean reaction norm of each subpopulation is anchored at the optimum genotypic value in its focal habitat. Linear reaction norms are parallel if the conditional distribution of adults around the focal habitats is the same for each subpopulation. Adult migration and absence of zygote dispersal represents the ultimate structured population, each habitat playing the role of focal habitat. Absence of zygote dispersal requires that the flow of individuals through the habitats is used instead of the habitats’ frequencies in the prediction of the evolved reaction norm. Adult migration in absence of zygote dispersal leads to an evolved pattern of locally differentiated reaction norms with optimum genotypic value anchored in the focal habitat and, for linear reaction norms, parallel slopes.

Variable environments may result in the evolution of adaptive phenotypic plasticity when cues reliably indicate an appropriate phenotype-environment match. Although adaptive plasticity is well established for phenological traits expressed across environments, local differentiation in norms of reaction is less well studied. The switch from the production of regular fronds to overwintering 'turions' in the greater duckweed Spirodela polyrhiza is vital to fitness and is expressed as a norm of reaction induced by falling temperatures associated with the onset of winter. However, the optimal norm of reaction to temperature is expected to differ across latitudes. Here, we test the hypothesis that a gradient in the length and predictability of growing seasons across latitudes results in the evolution of reaction norms characterized by earlier turion production at higher latitudes. We test this by collecting S.polyrhiza from replicate populations across seven latitudes from Ontario to Florida and then assessing differentiation in thermal reaction norms of turion production along a common temperature gradient. As predicted, northern populations produce turions at a lower birth order and earlier; a significant latitude-by-temperature interaction suggests that reaction norm differentiation has occurred. Our results provide evidence of differentiation in reaction norms across latitudes in a phenological trait, and we discuss how the adaptive significance of this plasticity might be further tested.