Phenotypic plasticity in gene expression contributes to divergence of locally adapted populations of Fundulus heteroclitus

We examine the interaction between phenotypic plasticity and evolutionary adaptation using muscle gene expression levels among populations of the fish Fundulus heteroclitus acclimated to three temperatures. Our analysis reveals shared patterns of phenotypic plasticity due to thermal acclimation as well as non‐neutral patterns of variation among populations adapted to different thermal environments. For the majority of significant differences in gene expression levels, phenotypic plasticity and adaptation operate on different suites of genes. The subset of genes that demonstrate both adaptive differences and phenotypic plasticity, however, exhibit countergradient variation of expression. Thus, expression differences among populations counteract environmental effects, reducing the phenotypic differentiation between populations. Finally, gene‐by‐environment interactions among genes with non‐neutral patterns of expression suggest that the penetrance of adaptive variation depends on the environmental conditions experienced by the individual.     

Environmental change, phenotypic plasticity, and genetic compensation

When a species encounters novel environmental conditions, some phenotypic characters may develop differently than in the ancestral environment. Most environmental perturbations of development are likely to reduce fitness, and thus selection would usually be expected to favor genetic changes that restore the ancestral phenotype. I propose the term "genetic compensation" to refer to this form of adaptive evolution. Genetic compensation is a subset of genetic accommodation and the reverse of genetic assimilation. When genetic compensation has occurred along a spatial environmental gradient, the mean trait values of populations in different environments may be more similar in the field than when representatives of the same populations are raised in a common environment (i.e., countergradient variation). If compensation is complete, genetic divergence between populations may be cryptic, that is, not detectable in the field. Here I apply the concept of genetic compensation to three examples involving carotenoid-based sexual coloration and then use these and other examples to discuss the concept in a broader context. I show that genetic compensation may lead to a cryptic form of reproductive isolation between populations evolving in different environments, may explain some puzzling cases in which heritable traits exposed to strong directional selection fail to show the expected evolutionary response, and may complicate efforts to monitor populations for signs of environmental deterioration.     

Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.     

Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail

Understanding the genetic and environmental bases of phenotypic variation and how they covary on local and broad geographic scales is an important goal of evolutionary ecology. Such information can shed light on how organisms adapt to different and changing environments and how life-history trade-offs arise. Surveys of phenotypic variation in 25 Littorina obtusata populations across an approximately 400-km latitudinal gradient in the Gulf of Maine revealed pronounced clines. The shells of snails from northern habitats weighed less and were thinner and weaker in compression than those of conspecifics from southern habitats. In contrast, body size (as measured by soft tissue mass) followed an opposite pattern; northern snails weighed more than southern snails. A reciprocal transplant between a northern and southern habitat revealed substantial plasticity in shell form and body mass and their respective measures of growth. Southern snails transplanted to the northern habitat produced lighter, thinner shells and more body mass than controls raised in their native habitat. In contrast, northern snails transplanted to the southern site produced heavier, thicker shells and less body mass than controls raised in their native habitat. Patterns of final phenotypic variation for all traits were consistent with cogradient variation (i.e., a positive covariance between genetic and environmental influences). However, growth in shell traits followed a countergradient pattern (i.e., a negative covariance between genetic and environmental influences). Interestingly, body growth followed a cogradient pattern, which may reflect constraints imposed by cogradient variation in final shell size and thickness. This result suggests the existence of potential life-history trade-offs associated with increased shell production. Differences in L. obtusata shell form, body mass, and their respective measures of growth are likely induced by geographic differences in both water temperature and the abundance of an invading crab predator (Carcinus maenas). Water temperatures averaged 6.8 degrees C warmer during the transplant experiment and C. maenas abundance is greater in the southern Gulf of Maine. Because both increased water temperature and crab effluent affect shell form in the same way, future experiments are needed to determine the relative importance of each. Nevertheless, it is clear that phenotypic plasticity has an important role in producing geographic variation in L. obtusata shell form. Moreover, the evolution of phenotypic plasticity in L. obtusata and other marine gastropods may be driven by architectural constraints imposed by shell form on body mass and growth.     

Morphological variation over ontogeny and environments in resource polymorphic arctic charr (Salvelinus alpinus)

SUMMARY Natural selection requires genetically based phenotypic variation to facilitate its action and cause adaptive evolution. It has become increasingly recognized that morphological development can become canalized likely as a result of selection. However, it is largely unknown how selection may influence canalization over ontogeny and differing environments. Changes in environments or colonization of a novel one is expected to result in adaptive divergence from the ancestral population when selection favors a new phenotypic optimum. In turn, a novel environment may also expose variation previously hidden from natural selection. We tested for changes in phenotypic variation over ontogeny and environments among ecomorphs of Arctic charr (Salvelinus alpinus) from two Icelandic lakes. Populations represented varying degrees of ecological specialization, with one lake population possessing highly specialized ecomorphs exhibiting a large degree of phenotypic divergence, whereas the other displayed more subtle divergence with more ecological overlap. Here we show that ecomorphs hypothesized to be the most specialized in each lake possess significant reductions in shape variation over ontogeny regardless of environmental treatment suggesting canalized development. However, environments did change the amount of shape variation expressed in these ecomorphs, with novel environments slowing the rate at which variation was reduced over ontogeny. Thus, environmental conditions may play an important role in determining the type and amount of genetically based phenotypic variation exposed to natural selection.     

Genetic,phenotypic, and environmental correlations in black medic,Medicago lupulina L., grown in three different environments

We have investigated the relationship between phenotypic and genetic correlations among a large number of quantitative traits (36) in three different environments in order to determine their degree of disparity and whether phenotypic correlations could be substituted for their genetic counterparts whatever the environment. We also studied the influence of the environment on genetic and phenotypic correlations. Twenty accessions (full-sib families) ofMedicago luPulina were grown in three environments. In two of these two levels of environmental stress were generated by harvesting plants at flowering and by growing plants in competition with barley, respectively. A third environment, with no treatment, was used as a control with no stress. Average values of pod and shoot weight indicate that competition induces the highest level of stress. The genetic and phenotypic correlations among the 36 traits were compared. Significant phenotypic correlations were obtained easily, while there was no genetic variation for 1 or the 2 characters being correlated. The large positive correlation between the genetic and phenotypic correlation matrices indicated a good proportionality between genetic and phenotypic correlations matrices but not their similarity. In a given environment, when only those traits with a significant genetic variance were taken into account, there were still differences between genetic and phenotypic correlations, even when levels of significance for phenotypic correlations were lowered. Consequently, it is dangerous to substitute phenotypic correlations for genetic correlations. The number of traits that showed genetic variability increased with increasing environmental stress, consequently the number of significant genetic correlations also increased with increasing environmental stress. In contrast, the number of significant phenotypic correlations was not influnced by the environment. The structures of both phenotypic and genetic matrices, however, depended on the environment, and not in the same way for both matrices.     

The roles of pre‐ and post‐hatching growth rates in generating a latitudinal cline of body size in the eastern fence lizard (Sceloporus undulatus)

Countergradient variation in norms of reaction can dampen the direct effects of environmental influences on phenotypic traits, allowing phenotypic similarity among populations despite exposure to different environmental conditions. Such norms of reaction may occur at any phase of the life‐history (e.g. growth rates during both embryonic and postembryonic stages may influence geographical variation in adult body size). We collected gravid female lizards (Sceloporus undulatus) from northern (Indiana), central (Mississippi), and southern (Florida) populations, spanning almost the full latitudinal range of the species. Adult females from the southern population were smaller. Intrinsic growth rates of hatchlings were higher for the central population than for the other two populations. This pattern does not parallel the countergradient variation previously found in embryonic developmental rates among these populations. Earlier hatching enhanced survival rates of juveniles to a similar degree among populations, although juvenile survival rates in the field generally increase with latitude in this species. Our data reveal geographical variation in the ways in which intrinsic developmental/growth rates and survival shift during ontogeny, and suggest that latitudinal patterns in adult body size (such as Bergmann's rule) can result from both faster growth, and longer periods of growth. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 202–209.     

The role of changes in environmental quality in multitrait plastic responses to environmental and social change in the model microalga Chlamydomonas reinhardtii

Intraspecific variation plays a key role in species'' responses to environmental change; however, little is known about the role of changes in environmental quality (the population growth rate an environment supports) on intraspecific trait variation. Here, we hypothesize that intraspecific trait variation will be higher in ameliorated environments than in degraded ones. We first measure the range of multitrait phenotypes over a range of environmental qualities for three strains and two evolutionary histories of Chlamydomonas reinhardtii in laboratory conditions. We then explore how environmental quality and trait variation affect the predictability of lineage frequencies when lineage pairs are grown in indirect co‐culture. Our results show that environmental quality has the potential to affect intraspecific variability both in terms of the variation in expressed trait values, and in terms of the genotype composition of rapidly growing populations. We found low phenotypic variability in degraded or same‐quality environments and high phenotypic variability in ameliorated conditions. This variation can affect population composition, as monoculture growth rate is a less reliable predictor of lineage frequencies in ameliorated environments. Our study highlights that understanding whether populations experience environmental change as an increase or a decrease in quality relative to their recent history affects the changes in trait variation during plastic responses, including growth responses to the presence of conspecifics. This points toward a fundamental role for changes in overall environmental quality in driving phenotypic variation within closely related populations, with implications for microevolution.     

Plasticity and evolution in correlated suites of traits

When organisms are faced with new or changing environments, a central challenge is the coordination of adaptive shifts in many different phenotypic traits. Relationships among traits may facilitate or constrain evolutionary responses to selection, depending on whether the direction of selection is aligned or opposed to the pattern of trait correlations. Attempts to predict evolutionary potential in correlated traits generally assume that correlations are stable across time and space; however, increasing evidence suggests that this may not be the case, and flexibility in trait correlations could bias evolutionary trajectories. We examined genetic and environmental influences on variation and covariation in a suite of behavioural traits to understand if and how flexibility in trait correlations influences adaptation to novel environments. We tested the role of genetic and environmental influences on behavioural trait correlations by comparing Trinidadian guppies (Poecilia reticulata) historically adapted to high‐ and low‐predation environments that were reared under native and non‐native environmental conditions. Both high‐ and low‐predation fish exhibited increased behavioural variance when reared under non‐native vs. native environmental conditions, and rearing in the non‐native environment shifted the major axis of variation among behaviours. Our findings emphasize that trait correlations observed in one population or environment may not predict correlations in another and that environmentally induced plasticity in correlations may bias evolutionary divergence in novel environments.     

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.     

Microgeographic countergradient variation in the wood frog, Rana sylvatica

Prior studies have shown that macrogeographic gradients in temperature associated with latitude and altitude can lead to countergradient patterns of variation in a number of taxa: individuals from colder environments are known to grow or develop faster than their conspecifics from warmer environments when placed in a common setting. In this study, I hypothesized that countergradient variation also is important at microgeographic scales. The wood frog, Rana sylvatica, breeds in open-canopied, temporary wetlands as well as those heavily shaded by vegetation. Shading leads to cooler thermal environments that are associated with embryonic development rates as much as 50% slower than those in unshaded wetlands. Wetlands with contrasting canopy environments are often found within tens or hundreds of meters of each other. In a common garden experiment, embryos from nearby natural wetlands displayed countergradient variation: individuals collected from shaded wetlands developed up to 12% faster than those collected from relatively unshaded wetlands. The results of this study suggest that the concept of countergradient variation may be extended to small scales of space. In addition, the rate and scale of vegetation dynamics (the agent of wetland shading) imply that divergence in development among residents of nearby wetlands may be relatively rapid, on the order of decades.     

Eco-evolutionary dynamics: disentangling phenotypic,environmental and population fluctuations

Decomposing variation in population growth into contributions from both ecological and evolutionary processes is of fundamental concern, particularly in a world characterized by rapid responses to anthropogenic threats. Although the impact of ecological change on evolutionary response has long been acknowledged, the converse has predominantly been neglected, especially empirically. By applying a recently published conceptual framework, we assess and contrast the relative importance of phenotypic and environmental variability on annual population growth in five ungulate populations. In four of the five populations, the contribution of phenotypic variability was greater than the contribution of environmental variability, although not significantly so. The similarity in the contributions of environment and phenotype suggests that neither is worthy of neglect. Population growth is a consequence of multiple processes, which strengthens arguments advocating integrated approaches to assess how populations respond to their environments.     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

Latitudinal countergradient variation in the common frog (Rana temporaria) development rates--evidence for local adaptation

Adaptive genetic differentiation along a climatic gradient as a response to natural selection is not necessarily expressed at phenotypic level if environmental effects on population mean phenotypes oppose the genotypic effects. This form of cryptic evolution--called countergradient variation--has seldom been explicitly demonstrated for terrestrial vertebrates. We investigated the patterns of phenotypic and genotypic differentiation in developmental rates of common frogs (Rana temporaria) along a ca. 1600 km latitudinal gradient across Scandinavia. Developmental rates in the field were not latitudinally ordered, but displayed large variation even among different ponds within a given latitudinal area. In contrast, development rates assessed in the laboratory increased strongly and linearly with increasing latitude, suggesting a genetic capacity for faster development in the northern than the southern larvae. Experiments further revealed that environmental effects (temperature and food) could easily override the genetic effects on developmental rates, providing a possible mechanistic explanation as to why the genetic differentiation was not seen in the samples collected from the wild. Our results suggest that the higher developmental rates of the northern larvae are likely to be related to selection stemming from seasonal time constrains, rather than from selection dictated by low ambient temperatures per se. All in all, the results provide a demonstration of environmental effects concealing substantial latitudinally ordered genetic differentiation understandable in terms of adaptation to clinal variation in time constrains.     

Evidence for intraspecific phenotypic variation in songbirds along elevation gradients in central Europe

Studying phenotypic variations along gradients may provide insights into mechanisms that drive species distributions and thus can be useful indicators of environmental change. In mountains, the study of phenotypic variation along elevation gradients is of increasing relevance due to the impacts of climate change. We analysed European ringing data to measure the direction of phenotypic variation along elevation gradients in six common, resident songbird species occurring along a wide elevational range. We modelled intraspecific change in wing length, body mass and their ratio with elevation and found a significant increase in wing length and a decrease in body mass at high elevations. The results of our exploratory analysis show the potential that continent-wide ringing databases offer to describe patterns of phenotypic variation along environmental gradients.     

HOW STABLE ‘SHOULD’ EPIGENETIC MODIFICATIONS BE? INSIGHTS FROM ADAPTIVE PLASTICITY AND BET HEDGING

Although there is keen interest in the potential adaptive value of epigenetic variation, it is unclear what conditions favor the stability of these variants either within or across generations. Because epigenetic modifications can be environmentally sensitive, existing theory on adaptive phenotypic plasticity provides relevant insights. Our consideration of this theory suggests that stable maintenance of environmentally induced epigenetic states over an organism's lifetime is most likely to be favored when the organism accurately responds to a single environmental change that subsequently remains constant, or when the environmental change cues an irreversible developmental transition. Stable transmission of adaptive epigenetic states from parents to offspring may be selectively favored when environments vary across generations and the parental environment predicts the offspring environment. The adaptive value of stability beyond a single generation of parent–offspring transmission likely depends on the costs of epigenetic resetting. Epigenetic stability both within and across generations will also depend on the degree and predictability of environmental variation, dispersal patterns, and the (epi)genetic architecture underlying phenotypic responses to environment. We also discuss conditions that favor stability of random epigenetic variants within the context of bet hedging. We conclude by proposing research directions to clarify the adaptive significance of epigenetic stability.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.     

Variation in mitochondrial DNA in a cline of allele frequencies and shell phenotype in the dog-whelk Nucella lapillus (L.)

Genetic constitution in the intertidal gastropod Nucella lapillus (L.) influences shell shape, growth rate and physiology. Clinal variation in these traits along a 5 km stretch of coastline in south Devon can be related to environmental variation in temperature and desiccation stress. We have examined mtDNA variation along this shore to investigate whether the cline represents primary or secondary contact. Two distinct mtDNA haplotypes were found which exhibit coincident step clines with karyotypic, allozymic and phenotypic variation and covary with the environmental pressures of temperature and desiccation. These results are interpreted in the context of the wider scale distribution of genetic and phenotypic variation in N. lapillus. It is suggested that the shore studied may represent one of a number of regions of secondary contact within a mosaic hybrid zone in N. lapillus , where coadapted phenotypic variation correlates with habitat and the position of the clines represents an environmental transition.     

Phenotypic consequences of genetic variation in a gynogenetic complex of Phoxinus eos-neogaeus clonal fish (Pisces: Cyprinidae) inhabiting a heterogeneous environment

We examined the genetic composition, habitat use, and morphological variation of a Phoxinus eos-neogaeus unisexual hybrid complex and its sexually reproducing progenitor species inhabiting beaver-modified drainages of Voyageurs National Park, Minnesota. In addition to the single diploid P. eos-neogaeus gynogenetic clone, triploid and diploid-triploid mosaic biotypes were present at our study sites. Both P. eos and P. neogaeus, and all three hybrid biotypes were ubiquitous throughout one intensively surveyed drainage, but abundances and relative frequencies of the parental species and hybrids varied considerably within and among successional environments. Data from a large number of additional sites indicated that the proportion of polyploid hybrids within an environment was negatively related to hybrid relative frequency, implying that the genomic constitution of hybrids is an important determinant of clonal fitness among successional environments. Statistical comparisons of variation along size-free multivariate body shape axes indicated that despite its genetic uniformity, the P. eos-neogaeus clone is no less variable than its sexual progenitors, suggesting that a single genotype may actually respond to environmental variation with as much phenotypic variation as a genetically variable sexual population. The incorporation and expression of a third genome in triploid and diploid-triploid mosaic biotypes derived from the gynogenetic clone significantly expanded phenotypic variation of the clone. This additional variation results in greater similarities in habitat use and morphological overlap with the parental species, primarily P. eos, the predominant sperm donor for gynogenetic hybrid females in this complex. Polyploid augmentation of a diploid gynogenetic clone appears to be typical in the P. eos-neogaeus complex, and the additional genetic and phenotypic variation that it generates has potentially significant ecological and evolutionary consequences for the success and persistence of a single genotype in highly variable environments.