Ontogenetic changes in genetic variances of age-dependent plasticity along a latitudinal gradient

The expression of phenotypic plasticity may differ among life stages of the same organism. Age-dependent plasticity can be important for adaptation to heterogeneous environments, but this has only recently been recognized. Whether age-dependent plasticity is a common outcome of local adaptation and whether populations harbor genetic variation in this respect remains largely unknown. To answer these questions, we estimated levels of additive genetic variation in age-dependent plasticity in six species of damselflies sampled from 18 populations along a latitudinal gradient spanning 3600 km. We reared full sib larvae at three temperatures and estimated genetic variances in the height and slope of thermal reaction norms of body size at three points in time during ontogeny using random regression. Our data show that most populations harbor genetic variation in growth rate (reaction norm height) in all ontogenetic stages, but only some populations and ontogenetic stages were found to harbor genetic variation in thermal plasticity (reaction norm slope). Genetic variances in reaction norm height differed among species, while genetic variances in reaction norm slope differed among populations. The slope of the ontogenetic trend in genetic variances of both reaction norm height and slope increased with latitude. We propose that differences in genetic variances reflect temporal and spatial variation in the strength and direction of natural selection on growth trajectories and age-dependent plasticity. Selection on age-dependent plasticity may depend on the interaction between temperature seasonality and time constraints associated with variation in life history traits such as generation length.     

VARIATION IN THERMAL PERFORMANCE AND REACTION NORMS AMONG POPULATIONS OF DROSOPHILA MELANOGASTER

The major goal of evolutionary thermal biology is to understand how variation in temperature shapes phenotypic evolution. Comparing thermal reaction norms among populations from different thermal environments allows us to gain insights into the evolutionary mechanisms underlying thermal adaptation. Here, we have examined thermal adaptation in six wild populations of the fruit fly (Drosophila melanogaster) from markedly different natural environments by analyzing thermal reaction norms for fecundity, thorax length, wing area, and ovariole number under ecologically realistic fluctuating temperature regimes in the laboratory. Contrary to expectation, we found only minor differences in the thermal optima for fecundity among populations. Differentiation among populations was mainly due to differences in absolute (and partly also relative) thermal fecundity performance. Despite significant variation among populations in the absolute values of morphological traits, we observed only minor differentiation in their reaction norms. Overall, the thermal reaction norms for all traits examined were remarkably similar among different populations. Our results therefore suggest that thermal adaptation in D. melanogaster predominantly involves evolutionary changes in absolute trait values rather than in aspects of thermal reaction norms.     

Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment

Phenotypic plasticity may allow species to cope with environmental variation. The study of thermal plasticity and its evolution helps understanding how populations respond to variation in temperature. In the context of climate change, it is essential to realize the impact of historical differences in the ability of populations to exhibit a plastic response to thermal variation and how it evolves during colonization of new environments. We have analyzed the real‐time evolution of thermal reaction norms of adult and juvenile traits in Drosophila subobscura populations from three locations of Europe in the laboratory. These populations were kept at a constant temperature of 18ºC, and were periodically assayed at three experimental temperatures (13ºC, 18ºC, and 23ºC). We found initial differentiation between populations in thermal plasticity as well as evolutionary convergence in the shape of reaction norms for some adult traits, but not for any of the juvenile traits. Contrary to theoretical expectations, an overall better performance of high latitude populations across temperatures in early generations was observed. Our study shows that the evolution of thermal plasticity is trait specific, and that a new stable environment did not limit the ability of populations to cope with environmental challenges.     

Microgeographic variation in temperature-induced plasticity in an isolated amphibian metapopulation

Variation in local environments may lead to variation in the selection pressures and differentiation among local populations even at microgeographic scale. We investigated variation in temperature-induced plasticity in larval life-history traits among populations of an isolated pool frog (Rana lessonae) metapopulation in Central Sweden. Successful breeding of this northern fringe metapopulation is highly dependent on early summer temperature, however, the metapopulation shows very little variation in molecular genetic markers suggesting limited potential for local differentiation. We exposed larvae from three closely-located populations to two temperatures (20 and 25°C) in laboratory to investigate their growth and development responses to temperature variation. In general, larvae exposed to warmer temperature experienced higher survival and metamorphosed faster, but at a smaller size than those at low temperature. We found differences among the populations in both trait mean values and in the plastic responses. Among-family variation within populations was found in growth rate and time to metamorphosis, as well as in plasticity suggesting that these traits have a capacity to evolve. Our results indicate ample phenotypic variation within and among these closely-located populations despite the low molecular genetic variation. The differences in pond temperature characteristics detected in the study in the three localities may suggest that differential selection is acting in the populations. The strong differentiation found in the larval traits implies that understanding the factors that influence the potential of the populations to adapt to environmental changes may be essential for successful conservation strategies.     

Old wine in new bottles: reaction norms in salmonid fishes

Genetic variability in reaction norms reflects differences in the ability of individuals, populations and ultimately species to respond to environmental change. By increasing our understanding of how genotype × environment interactions influence evolution, studies of genetic variation in phenotypic plasticity serve to refine our capacity to predict how populations will respond to natural and anthropogenic environmental variability, including climate change. Given the extraordinary variability in morphology, behaviour and life history in salmonids, one might anticipate the research milieu on reaction norms in these fishes to be empirically rich and intellectually engaging. Here, I undertake a review of genetic variability in continuous and discontinuous (threshold) norms of reaction in salmonid fishes, as determined primarily (but not exclusively) by common-garden experiments. Although in its infancy from a numerical publication perspective, there is taxonomically broad evidence of genetic differentiation in continuous, threshold and bivariate reaction norms among individuals, families and populations (including inter-population hybrids and backcrosses) for traits as divergent as embryonic development, age and size at maturity, and gene expression. There is compelling inferential evidence that plasticity is heritable and that population differences in reaction norms can reflect adaptive responses, by natural selection, to local environments. As a stimulus for future work, a series of 20 research questions are identified that focus on reaction-norm variability, selection, costs and constraints, demographic and conservation consequences, and genetic markers and correlates of phenotypic plasticity.     

Local adaptation in brown trout early life-history traits: implications for climate change adaptability

Knowledge of local adaptation and adaptive potential of natural populations is becoming increasingly relevant due to anthropogenic changes in the environment, such as climate change. The concern is that populations will be negatively affected by increasing temperatures without the capacity to adapt. Temperature-related adaptability in traits related to phenology and early life history are expected to be particularly important in salmonid fishes. We focused on the latter and investigated whether four populations of brown trout (Salmo trutta) are locally adapted in early life-history traits. These populations spawn in rivers that experience different temperature conditions during the time of incubation of eggs and embryos. They were reared in a common-garden experiment at three different temperatures. Quantitative genetic differentiation (QST) exceeded neutral molecular differentiation (FST) for two traits, indicating local adaptation. A temperature effect was observed for three traits. However, this effect varied among populations due to locally adapted reaction norms, corresponding to the temperature regimes experienced by the populations in their native environments. Additive genetic variance and heritable variation in phenotypic plasticity suggest that although increasing temperatures are likely to affect some populations negatively, they may have the potential to adapt to changing temperature regimes.     

Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature-size rule

The temperature-size rule is a common pattern of phenotypic plasticity in which higher temperature during development results in a smaller adult body size (i.e. a thermal reaction norm with negative slope). Examples and exceptions to the rule are known in multiple groups of organisms, but rapid population differentiation in the temperature-size rule has not been explored. Here we examine the genetic and parental contributions to population differentiation in thermal reaction norms for size, development time and survival in the Cabbage White Butterfly Pieris rapae, for two geographical populations that have likely diverged within the past 150 years. We used split-sibship experiments with two temperature treatments (warm and cool) for P. rapae from Chapel Hill, NC, and from Seattle, WA. Mixed-effect model analyses demonstrate significant genetic differences between NC and WA populations for adult size and for thermal reaction norms for size. Mean adult mass was 12-24% greater in NC than in WA populations for both temperature treatments; mean size was unaffected or decreased with temperature (the temperature-size rule) for the WA population, but size increased with temperature for the NC population. Our study shows that the temperature-size rule and related thermal reaction norms can evolve rapidly within species in natural field conditions. Rapid evolutionary divergence argues against the existence of a simple, general mechanistic constraint as the underlying cause of the temperature-size rule.     

Role of phenotypic plasticity and population differentiation in adaptation to novel environmental conditions

Species can adapt to new environmental conditions either through individual phenotypic plasticity, intraspecific genetic differentiation in adaptive traits, or both. Wild emmer wheat, Triticum dicoccoides, an annual grass with major distribution in Eastern Mediterranean region, is predicted to experience in the near future, as a result of global climate change, conditions more arid than in any part of the current species distribution. To understand the role of the above two means of adaptation, and the effect of population range position, we analyzed reaction norms, extent of plasticity, and phenotypic selection across two experimental environments of high and low water availability in two core and two peripheral populations of this species. We studied 12 quantitative traits, but focused primarily on the onset of reproduction and maternal investment, which are traits that are closely related to fitness and presumably involved in local adaptation in the studied species. We hypothesized that the population showing superior performance under novel environmental conditions will either be genetically differentiated in quantitative traits or exhibit higher phenotypic plasticity than the less successful populations. We found the core population K to be the most plastic in all three trait categories (phenology, reproductive traits, and fitness) and most successful among populations studied, in both experimental environments; at the same time, the core K population was clearly genetically differentiated from the two edge populations. Our results suggest that (1) two means of successful adaptation to new environmental conditions, phenotypic plasticity and adaptive genetic differentiation, are not mutually exclusive ways of achieving high adaptive ability; and (2) colonists from some core populations can be more successful in establishing beyond the current species range than colonists from the range extreme periphery with conditions seemingly closest to those in the new environment.     

The genetics of phenotypic plasticity. IX. Genetic architecture, temperature, and sex differences in Drosophila melanogaster

Abstract.— We examined the genetic architecture of plasticity of thorax and wing length in response to temperature in Drosophila melanogaster . Reaction norms as a function of growth temperature were analyzed in 20 isofemale lines in a natural population collected from Grande Ferrade near Bordeaux (southern France) in two different years. We found evidence for a complex genetic architecture underlying the reaction norms and differences between males and females. Reaction norms were negative quadratics. Genetic correlations were moderately high between traits within environments. Among characteristic values, the magnitudes of genetic correlations varied among traits and sexes. We hypothesized that genetic correlations among environments would decrease as temperatures became more different. This expectation was upheld for only one trait, female thorax length. For males for both traits, the correlations were large for both very similar and very different temperatures. These correlations may constrain the evolution of the shape of the reaction norms. Whether the extent of independence implies specific regulatory genes or only a specific allelic regulation of trait genes can not be decided from our results.     

Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity

Variation in body size, growth and life history traits of ectotherms along latitudinal and altitudinal clines is generally assumed to represent adaptation to local environmental conditions, especially adaptation to temperature. However, the degree to which variation along these clines is due to adaptation vs plasticity remains poorly understood. In addition, geographic patterns often differ between females and males – e.g. sexual dimorphism varies along latitudinal clines, but the extent to which these sex differences are due to genetic differences between sexes vs sex differences in plasticity is poorly understood. We use common garden experiments (beetles reared at 24, 30 and 36°C) to quantify the relative contribution of genetically‐based differentiation among populations vs phenotypic plasticity to variation in body size and other traits among six populations of the seed‐feeding beetle Stator limbatus collected from various altitudes in Arizona, USA. We found that temperature induces substantial plasticity in survivorship, body size and female lifetime fecundity, indicating that developmental temperature significantly affects growth and life history traits of S. limbatus. We also detected genetic differences among populations for body size and fecundity, and genetic differences among populations in thermal reaction norms, but the altitude of origin (and hence mean temperature) does not appear to explain these genetic differences. This and other recent studies suggest that temperature is not the major environmental factor that generates geographic variation in traits of this species. In addition, though there was no overall difference in plasticity of body size between males and females (when averaged across populations), we did find that the degree to which dimorphism changed with temperature varied among populations. Consequently, future studies should be extremely cautious when using only a few study populations to examine environmental effects on sexual dimorphism.     

VARIATION IN REACTION NORMS AMONG POPULATIONS OF THE GRASS BOUTELOUA RIGIDISETA

Recent research has emphasized the importance of investigating the reaction norms of quantitative traits to understand evolution in natural environments. In this study, genetic differences in reaction norms among eight populations of the grass Bouteloua rigidiseta were examined using clonal replicates of genotypes planted in a common garden with two levels of competition (single B. rigidiseta without competition and single B. rigidiseta surrounded by four Erioneuron pilosum). The populations were found to be genetically differentiated for a variety of traits. Differences in reaction norms of size-specific fecundity (spikelet clusters per tiller number) were detected among the populations: some showed little response to competition; in others size-specific fecundity was much greater in the absence of competition. This divergence in reaction norms among these populations may be the result of past selection (including the cost of plasticity), or genetic drift.     

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.     

The ubiquity of phenotypic plasticity in plants: a synthesis

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.     

Land use causes genetic differentiation of life‐history traits in Bromus hordeaceus

There is increasing evidence that species can evolve rapidly in response to environmental change. However, although land use is one of the key drivers of current environmental change, studies of its evolutionary consequences are still fairly scarce, in particular studies that examine land‐use effects across large numbers of populations, and discriminate between different aspects of land use. Here, we investigated genetic differentiation in relation to land use in the annual grass Bromus hordeaceus. A common garden study with offspring from 51 populations from three regions and a broad range of land‐use types and intensities showed that there was indeed systematic population differentiation of ecologically important plant traits in relation to land use, in particular due to increasing mowing and grazing intensities. We also found strong land‐use‐related genetic differentiation in plant phenology, where the onset of flowering consistently shifted away from the typical time of management. In addition, increased grazing intensity significantly increased the genetic variability within populations. Our study suggests that land use can cause considerable genetic differentiation among plant populations, and that the timing of land use may select for phenological escape strategies, particularly in monocarpic plant species.     

CHARACTERIZING SELECTION ON PHENOTYPIC PLASTICITY IN RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal‐scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full‐sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full‐sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes.     

Development time and size-related traits in the oriental blowfly, Chrysomya megacephala along a latitudinal gradient from China

Organisms can respond to variation in temperature through the direct effect of temperature on phenotypes (phenotypic plasticity), or through long-term adaptation to temperature (and thus evolution of either mean size or thermal reaction norm). We examined the effects of various temperatures (of 20 and 30 °C) on development time, adult body size (body length and body width) and pre-adult survivorship in six populations of Chrysomya megacephala, collected at different latitudes. We found that temperature changes induced substantial plasticity in terms of development time, body size and pre-adult survivorship, indicating that developmental temperature significantly affects growth and life history traits of C. megacephala. We also detected genetic differences among populations for body size and development time, and these two traits exhibited highly significant variations in the responses of different populations to various temperature conditions, indicating genetic differences among populations in terms of thermal reaction norms. The latitude of origin of the different populations (and hence mean temperature regimes in the environments from where the populations originated) did not appear to fully explain these genetic differences. In short, changes in development time and body size in C. megacephala can be regarded as adaptations to changing thermal regimes.     

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.