Genetic variation in life-history reaction norms in a marine fish

Neither the scale of adaptive variation nor the genetic basis for differential population responses to the environment is known for broadcast-spawning marine fishes. Using a common-garden experimental protocol, we document how larval growth, survival and their norms of reaction differ genetically among four populations of Atlantic cod (Gadus morhua). These traits, and their plastic responses to food and temperature, differed across spatial scales at which microsatellite DNA failed to detect population structure. Divergent survival reaction norms indicate that warm-water populations are more sensitive to changes in food, whereas cold-water populations are more sensitive to changes in temperature. Our results suggest that neither the direction nor the magnitude of demographic responses to environmental change need be the same among populations. Adaptive phenotypic plasticity, previously undocumented in marine fishes, can significantly influence the probability of recovery and persistence of collapsed populations by affecting their ability to respond to natural and anthropogenic environmental change.     

When three traits make a line: evolution of phenotypic plasticity and genetic assimilation through linear reaction norms in stochastic environments

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.     

Stressful environments induce novel phenotypic variation: hierarchical reaction norms for sperm performance of a pervasive invader

Genetic variation for phenotypic plasticity is ubiquitous and important. However, the scale of such variation including the relative variability present in reaction norms among different hierarchies of biological organization (e.g., individuals, populations, and closely related species) is unknown. Complicating interpretation is a trade‐off in environmental scale. As plasticity can only be inferred over the range of environments tested, experiments focusing on fine tuned responses to normal or benign conditions may miss cryptic phenotypic variation expressed under novel or stressful environments. Here, we sought to discern the presence and shape of plasticity in the performance of brown trout sperm as a function of optimal to extremely stressful river pH, and demarcate if the reaction norm varies among genotypes. Our overarching goal was to determine if deteriorating environmental quality increases expressed variation among individuals. A more applied aim was to ascertain whether maintaining sperm performance over a wide pH range could help explain how brown trout are able to invade diverse river systems when transplanted outside of their native range. Individuals differed in their reaction norms of phenotypic expression of an important trait in response to environmental change. Cryptic variation was revealed under stressful conditions, evidenced through increasing among‐individual variability. Importantly, data on population averages masked this variability in plasticity. In addition, canalized reaction norms in sperm swimming velocities of many individuals over a very large range in water chemistry may help explain why brown trout are able to colonize a wide variety of habitats.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

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

Populations adapt to novel environmental conditions by genetic changes or phenotypic plasticity. Plastic responses are generally faster and can buffer fitness losses under variable conditions. Plasticity is typically modeled as random noise and linear reaction norms that assume simple one‐to‐one genotype–phenotype maps and no limits to the phenotypic response. Most studies on plasticity have focused on its effect on population viability. However, it is not clear, whether the advantage of plasticity depends solely on environmental fluctuations or also on the genetic and demographic properties (life histories) of populations. Here we present an individual‐based model and study the relative importance of adaptive and nonadaptive plasticity for populations of sexual species with different life histories experiencing directional stochastic climate change. Environmental fluctuations were simulated using differentially autocorrelated climatic stochasticity or noise color, and scenarios of directional climate change. Nonadaptive plasticity was simulated as a random environmental effect on trait development, while adaptive plasticity as a linear, saturating, or sinusoidal reaction norm. The last two imposed limits to the plastic response and emphasized flexible interactions of the genotype with the environment. Interestingly, this assumption led to (a) smaller phenotypic than genotypic variance in the population (many‐to‐one genotype–phenotype map) and the coexistence of polymorphisms, and (b) the maintenance of higher genetic variation—compared to linear reaction norms and genetic determinism—even when the population was exposed to a constant environment for several generations. Limits to plasticity led to genetic accommodation, when costs were negligible, and to the appearance of cryptic variation when limits were exceeded. We found that adaptive plasticity promoted population persistence under red environmental noise and was particularly important for life histories with low fecundity. Populations producing more offspring could cope with environmental fluctuations solely by genetic changes or random plasticity, unless environmental change was too fast.     

Mixed support for an alignment between phenotypic plasticity and genetic differentiation in damselfly wing shape

The relationship between genetic differentiation and phenotypic plasticity can provide information on whether plasticity generally facilitates or hinders adaptation to environmental change. Here, we studied wing shape variation in a damselfly (Lestes sponsa) across a latitudinal gradient in Europe that differed in time constraints mediated by photoperiod and temperature. We reared damselflies from northern and southern populations in the laboratory using a reciprocal transplant experiment that simulated time-constrained (i.e. northern) and unconstrained (southern) photoperiods and temperatures. After emergence, adult wing shape was analysed using geometric morphometrics. Wings from individuals in the northern and southern populations differed significantly in shape when animals were reared in their respective native environment. Comparing wing shape across environments, we found evidence for phenotypic plasticity in wing shape, and this response differed across populations (i.e. G × E interactions). This interaction was driven by a stronger plastic response by individuals from the northern population and differences in the direction of plastic wing shape changes among populations. The alignment between genetic and plastic responses depended on the specific combination of population and rearing environment. For example, there was an alignment between plasticity and genetic differentiation under time-constrained, but not under non-time-constrained conditions for forewings. We thus find mixed support for the hypothesis that environmental plasticity and genetic population differentiation are aligned. Furthermore, although our laboratory treatments mimicked the natural climatic conditions at northern and southern latitudes, the effects of population differences on wing shape were two to four times stronger than plastic effects. We discuss our results in terms of time constraints and the possibility that natural and sexual selection is acting differently on fore- and hindwings.     

Habitat-specific differences in thermal plasticity in natural populations of a soil arthropod

When populations experience substantial variation in environmental conditions, they may evolve phenotypic plasticity in response to these varying selection pressures. Evolutionary theory predicts differentiation in the level of phenotypic plasticity among different habitats. We evaluated temperature-induced phenotypic responses in juvenile growth rate in natural populations of the springtail Orchesella cincta , inhabiting forest and heathland. These habitats typically co-occur but differ strongly with respect to, for example, thermal regime, relative humidity, and structure. Offspring of females from the two habitats were reared at different temperatures in climate rooms and the temperature response of juvenile growth rate and egg size was measured. We found a habitat-specific difference in plasticity of juvenile growth rate. The reaction norms of the forest populations were steeper than the reaction norms for heath populations at two replicated sampling sites. Egg weight itself was demonstrated to be a plastic trait with a higher egg weight at low temperatures, but the thermal response did not differ between habitats. We conclude that these populations have diverged due to strong local natural selection. Our results support the argument that the level of phenotypic plasticity itself can be under selection and that differentiation in reaction norms can occur even in neighbouring habitats with no barrier to gene flow.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 265–271.     

PHENOTYPIC PLASTICITY AND EPIGENETIC MARKING: AN ASSESSMENT OF EVIDENCE FOR GENETIC ACCOMMODATION

The relationship between genotype (which is inherited) and phenotype (the target of selection) is mediated by environmental inputs on gene expression, trait development, and phenotypic integration. Phenotypic plasticity or epigenetic modification might influence evolution in two general ways: (1) by stimulating evolutionary responses to environmental change via population persistence or by revealing cryptic genetic variation to selection, and (2) through the process of genetic accommodation, whereby natural selection acts to improve the form, regulation, and phenotypic integration of novel phenotypic variants. We provide an overview of models and mechanisms for how such evolutionary influences may be manifested both for plasticity and epigenetic marking. We point to promising avenues of research, identifying systems that can best be used to address the role of plasticity in evolution, as well as the need to apply our expanding knowledge of genetic and epigenetic mechanisms to our understanding of how genetic accommodation occurs in nature. Our review of a wide variety of studies finds widespread evidence for evolution by genetic accommodation.     

Individual variation in thermal plasticity and its impact on mass-scaling

Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass-scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass-scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months (N_{[observations]} = 4952). Using hierarchical statistical techniques, we accounted for multi-level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass-scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (R_slope = 0.25, 95% CI = 2.48 × 10⁻⁸ – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross-temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass-scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.     

Phenotypic plasticity and population viability: the importance of environmental predictability

Phenotypic plasticity plays a key role in modulating how environmental variation influences population dynamics, but we have only rudimentary understanding of how plasticity interacts with the magnitude and predictability of environmental variation to affect population dynamics and persistence. We developed a stochastic individual-based model, in which phenotypes could respond to a temporally fluctuating environmental cue and fitness depended on the match between the phenotype and a randomly fluctuating trait optimum, to assess the absolute fitness and population dynamic consequences of plasticity under different levels of environmental stochasticity and cue reliability. When cue and optimum were tightly correlated, plasticity buffered absolute fitness from environmental variability, and population size remained high and relatively invariant. In contrast, when this correlation weakened and environmental variability was high, strong plasticity reduced population size, and populations with excessively strong plasticity had substantially greater extinction probability. Given that environments might become more variable and unpredictable in the future owing to anthropogenic influences, reaction norms that evolved under historic selective regimes could imperil populations in novel or changing environmental contexts. We suggest that demographic models (e.g. population viability analyses) would benefit from a more explicit consideration of how phenotypic plasticity influences population responses to environmental change.     

The evolution of tolerance to damage in Gentianella campestris: natural selection and the quantitative genetics of tolerance

In the framework of phenotypic plasticity, tolerance to browsing can be operationally defined as a norm of reaction comparing plant performance in undamaged and damaged conditions. Genetic variation in tolerance is then indicated by heterogeneity in the slopes of norms of reaction from a population. We investigated field gentian (Gentianella campestris) tolerance to damage in the framework of phenotypic plasticity using a sample of maternal lines from natural populations grown under common garden conditions and randomly split into either a control or an artificial clipping treatment. We found a diversity of tolerance norms of reaction at both the population and family level: the impacts of clipping ranged from poor tolerance (negative slope) to overcompensation (positive slope). We detected heterogeneity in tolerance norms of reaction in four populations. Similarly, we found a variety of plastic architectural responses to clipping and genetic variation in these responses in several populations. Overall, we found that the most tolerant populations were late flowering and also exhibit the greatest plastic increases in node (meristem) production in response to damage. We studied damage-imposed natural selection on plasticity in plant architecture in 10 of the sampled populations. In general, there was strong positive direct selection on final number of nodes for both control and clipped plants. However, the total selection on nodes (direct + indirect selection) within each treatment category depended heavily on the frequency of damage and cross-treatment genetic correlations in node production. In some cases, strong correlated responses to selection across the damage treatment led to total selection against nodes in the more rare environment. This could ultimately lead to the evolution of maladaptive phenotypes in one or both of the treatment categories. These results suggest that tolerance and a variety of architectural responses to damage may evolve by both direct and indirect responses to natural selection. While the present study demonstrates the potential importance of cross-treatment genetic correlations in directing the evolution of tolerance traits, such as branch or node production, we did not find any strong evidence of genetic trade-offs in candidate tolerance traits between undamaged and damaged conditions. This revised version was published online in July 2006 with corrections to the Cover Date.     

Selection on heritable seasonal phenotypic plasticity of body mass

The ability to cope with environmental change is fundamental to a species' evolution. Organisms can respond to seasonal environmental variation through phenotypic plasticity. The substantial plasticity in body mass of temperate species has often been considered a simple consequence of change in environmental quality, but could also have evolved as an adaptation to seasonality. We investigated the genetic basis of, and selection acting on, seasonal plasticity in body mass for wild bighorn sheep ewes (Ovis canadensis) at Ram Mountain, Alberta, under two contrasting environmental conditions. Heritability of plasticity, estimated as mass-specific summer and winter mass changes, was low but significant. The additive genetic variance component of relative summer mass change was greater under good environmental conditions (characterized by a population increase and high juvenile survival) than under poor conditions (population decrease and low juvenile survival). Additive genetic variance of relative winter mass change appeared independent of environmental conditions. We found evidence of selection on summer (relative) and winter (relative and absolute) mass change. For a given mass, more plastic individuals (with greater seasonal mass changes) achieve greater fitness through reproduction in the following year. However, genetic correlations between mass parameters were positive. Our study supports the hypothesis that seasonal plasticity in body mass in vertebrates is an adaptation that evolved under natural selection to cope with environmental variation but genetic correlations with other traits might limit its evolutionary potential.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

Trait‐specific consequences of inbreeding on adaptive phenotypic plasticity

Environmental changes may stress organisms and stimulate an adaptive phenotypic response. Effects of inbreeding often interact with the environment and can decrease fitness of inbred individuals exposed to stress more so than that of outbred individuals. Such an interaction may stem from a reduced ability of inbred individuals to respond plastically to environmental stress; however, this hypothesis has rarely been tested. In this study, we mimicked the genetic constitution of natural inbred populations by rearing replicate Drosophila melanogaster populations for 25 generations at a reduced population size (10 individuals). The replicate inbred populations, as well as control populations reared at a population size of 500, were exposed to a benign developmental temperature and two developmental temperatures at the lower and upper margins of their viable range. Flies developed at the three temperatures were assessed for traits known to vary across temperatures, namely abdominal pigmentation, wing size, and wing shape. We found no significant difference in phenotypic plasticity in pigmentation or in wing size between inbred and control populations, but a significantly higher plasticity in wing shape across temperatures in inbred compared to control populations. Given that the norms of reaction for the noninbred control populations are adaptive, we conclude that a reduced ability to induce an adaptive phenotypic response to temperature changes is not a general consequence of inbreeding and thus not a general explanation of inbreeding–environment interaction effects on fitness components.     

Ontogenetic and evolutionary effects of predation and competition on nine-spined stickleback (Pungitius pungitius) body size

1.?Individual- and population-level variation in body size and growth often correlates with many fitness traits. Predation and food availability are expected to affect body size and growth as important agents of both natural selection and phenotypic plasticity. How differences in predation and food availability affect body size/growth during ontogeny in populations adapted to different predation and competition regimes is rarely studied. 2.?Nine-spined stickleback (Pungitius pungitius) populations originating from habitats with varying levels of predation and competition are known to be locally adapted to their respective habitats in terms of body size and growth. Here, we studied how different levels of perceived predation risk and competition during ontogeny affect the reaction norms of body size and growth in (i) marine and pond populations adapted to different levels of predation and competition and (ii) different sexes. We reared nine-spined stickleback in a factorial experiment under two levels of perceived predation risk (present/absent) and competition (high/low food supply). 3.?We found divergence in the reaction norms at two levels: (i) predation-adapted marine stickleback had stronger reactions to predatory cues than intraspecific competition-adapted pond stickleback, the latter being more sensitive to available food than the marine fish and (ii) females reacting more strongly to the treatments than males. 4.?The repeated, habitat-dependent nature of the differences suggests that natural selection is the agent behind the observed patterns. Our results suggest that genetic adaptation to certain environmental factors also involves an increase in the range of expressible phenotypic plasticity. We found support for this phenomenon at two levels: (i) across populations driven by habitat type and (ii) within populations driven by sex.     

Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow

Divergent natural selection, adaptive divergence and gene flow may interact in a number of ways. Recent studies have focused on the balance between selection and gene flow in natural populations, and empirical work has shown that gene flow can constrain adaptive divergence, and that divergent selection can constrain gene flow. A caveat is that phenotypic diversification may be under the direct influence of environmental factors (i.e. it may be due to phenotypic plasticity), in addition to partial genetic influence. In this case, phenotypic divergence may occur between populations despite high gene flow that imposes a constraint on genetic divergence. Plasticity may dampen the effects of natural selection by allowing individuals to rapidly adapt phenotypically to new conditions, thus slowing adaptive genetic divergence. On the other hand, plasticity may promote future adaptive divergence by allowing populations to persist in novel environments. Plasticity may promote gene flow between selective regimes by allowing dispersers to adapt to alternate conditions, or high gene flow may result in the selection for increased plasticity. Here I expand frameworks for understanding relationships among selection, adaptation and gene flow to include the effects of phenotypic plasticity in natural populations, and highlight its importance in evolutionary diversification.     

Human influences on rates of phenotypic change in wild animal populations

Human activities can expose populations to dramatic environmental perturbations, which may then precipitate adaptive phenotypic change. We ask whether or not phenotypic changes associated with human-disturbed (anthropogenic) contexts are greater than those associated with more 'natural' contexts. Our meta-analysis is based on more than 3000 rates of phenotypic change in 68 'systems', each representing a given species in a particular geographical area. We find that rates of phenotypic change are greater in anthropogenic contexts than in natural contexts. This difference may be influenced by phenotypic plasticity - because it was evident for studies of wild-caught individuals (which integrate both genetic and plastic effects) but not for common-garden or quantitative genetic studies (which minimize plastic effects). We also find that phenotypic changes in response to disturbance can be remarkably abrupt, perhaps again because of plasticity. In short, humans are an important agent driving phenotypic change in contemporary populations. Although these changes sometimes have a genetic basis, our analyses suggest a particularly important contribution from phenotypic plasticity.     

Artificial selection on phenotypically plastic traits

Many phenotypes respond physiologically or developmentally to continuously distributed environmental variables such as temperature and nutritional quality. Information about phenotypic plasticity can be used to improve the efficiency of artificial selection. Here we show that the quantitative genetic theory for 'infinite-dimensional' traits such as reaction norms provides a natural framework to accomplish this goal. It is expected to improve selection responses by making more efficient use of information about environmental effects than do conventional methods. The approach is illustrated by deriving an index for mass selection of a phenotypically plastic trait. We suggest that the same approach could be extended directly to more general and efficient breeding schemes, such as those based on general best linear unbiased prediction. Methods for estimating genetic covariance functions are reviewed.     

Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America

Species can respond to environmental pressures through genetic and epigenetic changes and through phenotypic plasticity, but few studies have evaluated the relationships between genetic differentiation and phenotypic plasticity of plant species along changing environmental conditions throughout wide latitudinal ranges. We studied inter‐ and intrapopulation genetic diversity (using simple sequence repeats and chloroplast DNA sequencing) and inter‐ and intrapopulation phenotypic variability of 33 plant traits (using field and common‐garden measurements) for five populations of the invasive cordgrass Spartina densiflora Brongn. along the Pacific coast of North America from San Francisco Bay to Vancouver Island. Studied populations showed very low genetic diversity, high levels of phenotypic variability when growing in contrasted environments and high intrapopulation phenotypic variability for many plant traits. This intrapopulation phenotypic variability was especially high, irrespective of environmental conditions, for those traits showing also high phenotypic plasticity. Within‐population variation represented 84% of the total genetic variation coinciding with certain individual plants keeping consistent responses for three plant traits (chlorophyll b and carotenoid contents, and dead shoot biomass) in the field and in common‐garden conditions. These populations have most likely undergone genetic bottleneck since their introduction from South America; multiple introductions are unknown but possible as the population from Vancouver Island was the most recent and one of the most genetically diverse. S. densiflora appears as a species that would not be very affected itself by climate change and sea‐level rise as it can disperse, establish, and acclimate to contrasted environments along wide latitudinal ranges.