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.     

Trait Associations across Evolutionary Time within a Drosophila Phylogeny: Correlated Selection or Genetic Constraint?

Traits do not evolve independently. To understand how trait changes under selection might constrain adaptive changes, phenotypic and genetic correlations are typically considered within species, but these capture constraints across a few generations rather than evolutionary time. For longer-term constraints, comparisons are needed across species but associations may arise because of correlated selection pressures rather than genetic interactions. Implementing a unique approach, we use known patterns of selection to separate likely trait correlations arising due to correlated selection from those reflecting genetic constraints. We examined the evolution of stress resistance in >90 Drosophila species adapted to a range of environments, while controlling for phylogeny. Initially we examined the role of climate and phylogeny in shaping the evolution of starvation and body size, two traits previously not examined in this context. Following correction for phylogeny only a weak relationship between climate and starvation resistance was detected, while all of the variation in the relationship between body size and climate could be attributed to phylogeny. Species were divided into three environmental groups (hot and dry, hot and wet, cold) with the expectation that, if genetic correlations underpin trait correlations, these would persist irrespective of the environment, whereas selection-driven evolution should produce correlations dependent on the environment. We found positive associations between most traits in hot and dry environments coupled with high trait means. In contrast few trait correlations were observed in hot/wet and cold environments. These results suggest trait associations are primarily driven by correlated selection rather than genetic interactions, highlighting that such interactions are unlikely to limit evolution of stress resistance.     

HPA-axis activity in alcoholism: examples for a gene-environment interaction.

Genetic and environmental influences are both known to be causal factors in the development and maintenance of substance abuse disorders. This review aims to focus on the contributions of genetic and environmental research to the understanding of alcoholism and how gene-environment interactions result in a variety of addiction phenotypes. Gene-environment interactions have been reviewed by focusing on one of the most relevant environmental risk factors for alcoholism, stress. This is examined in more detail by reviewing the functioning of the hypothalamic-pituitary-adrenal (HPA) axis and its genetic and molecular components in this disorder. Recent evidence from animal and human studies have shown that the effects of stress on alcohol drinking are mediated by core HPA axis genes and are associated with genetic variations in those genes. The findings of the studies discussed here suggest that the collaborations of neuroscience, psychobiology and molecular genetics provide a promising framework to elucidate the exact mechanisms of gene-environment interactions as seen to convene upon the HPA axis and effect phenotypes of addiction.     

Variance components models for gene-environment interaction in twin analysis.

Gene-environment interaction is likely to be a common and important source of variation for complex behavioral traits. Often conceptualized as the genetic control of sensitivity to the environment, it can be incorporated in variance components twin analyses by partitioning genetic effects into a mean part, which is independent of the environment, and a part that is a linear function of the environment. The model allows for one or more environmental moderator variables (that possibly interact with each other) that may i). be continuous or binary ii). differ between twins within a pair iii). interact with residual environmental as well as genetic effects iv) have nonlinear moderating properties v). show scalar (different magnitudes) or qualitative (different genes) interactions vi). be correlated with genetic effects acting upon the trait, to allow for a test of gene-environment interaction in the presence of gene-environment correlation. Aspects and applications of a class of models are explored by simulation, in the context of both individual differences twin analysis and, in a companion paper (Purcell & Sham, 2002) sibpair quantitative trait locus linkage analysis. As well as elucidating environmental pathways, consideration of gene-environment interaction in quantitative and molecular studies will potentially direct and enhance gene-mapping efforts.     

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.     

Effects of data structure on the estimation of covariance functions to describe genotype by environment interactions in a reaction norm model

Covariance functions have been proposed to predict breeding values and genetic (co)variances as a function of phenotypic within herd-year averages (environmental parameters) to include genotype by environment interaction. The objective of this paper was to investigate the influence of definition of environmental parameters and non-random use of sires on expected breeding values and estimated genetic variances across environments. Breeding values were simulated as a linear function of simulated herd effects. The definition of environmental parameters hardly influenced the results. In situations with random use of sires, estimated genetic correlations between the trait expressed in different environments were 0.93, 0.93 and 0.97 while simulated at 0.89 and estimated genetic variances deviated up to 30% from the simulated values. Non random use of sires, poor genetic connectedness and small herd size had a large impact on the estimated covariance functions, expected breeding values and calculated environmental parameters. Estimated genetic correlations between a trait expressed in different environments were biased upwards and breeding values were more biased when genetic connectedness became poorer and herd composition more diverse. The best possible solution at this stage is to use environmental parameters combining large numbers of animals per herd, while losing some information on genotype by environment interaction in the data.     

Rapid changes in genetic architecture of behavioural syndromes following colonization of a novel environment

Behavioural syndromes, that is correlated behaviours, may be a result from adaptive correlational selection, but in a new environmental setting, the trait correlation might act as an evolutionary constraint. However, knowledge about the quantitative genetic basis of behavioural syndromes, and the stability and evolvability of genetic correlations under different ecological conditions, is limited. We investigated the quantitative genetic basis of correlated behaviours in the freshwater isopod Asellus aquaticus. In some Swedish lakes, A. aquaticus has recently colonized a novel habitat and diverged into two ecotypes, presumably due to habitat‐specific selection from predation. Using a common garden approach and animal model analyses, we estimated quantitative genetic parameters for behavioural traits and compared the genetic architecture between the ecotypes. We report that the genetic covariance structure of the behavioural traits has been altered in the novel ecotype, demonstrating divergence in behavioural correlations. Thus, our study confirms that genetic correlations behind behaviours can change rapidly in response to novel selective environments.     

Genetic correlations and their dependence on environmental similarity—Insights from livestock data

Genetic correlations for a trait across environments are predicted to decrease as environments diverge. However, estimates of genetic correlations from natural populations are typically defined across a limited environmental range and prone to very large standard errors, making it difficult to test this prediction. We address the importance of environmental distance on genetic correlations by employing data from domestic cattle in which abundant and accurate estimates are available from a wide range of environments. Three production traits related to milk yield show a clear decrease in genetic correlations with increasing environmental divergence. This pattern was also evident for growth traits and other yield traits but not for traits related to reproduction, morphology, physiology, or disease. We suspect that this reflects weaker selection on these latter trait classes compared to production traits, or alternatively the effects of selection are constrained by unfavorable genetic correlations between traits. The results support the notion that traits that historically have been under strong directional selection in a small range of frequently encountered environments will evolve high genetic correlations across these environments, while exposure to uncommon (and dissimilar) environments lead to a reranking of gene effects and a decrease in genetic correlations across environments.     

Non‐consumptive effects of predation: does perceived risk strengthen the genetic integration of behaviour and morphology in stickleback?

Predators can shape genetic correlations in prey by altering prey perception of risk. We manipulated perceived risk to test whether such non‐consumptive effects tightened behavioural trait correlations in wild‐caught stickleback from high‐ compared to low‐risk environments due to genetic variation in plasticity. We expected tighter genetic correlations within perceived risk treatments than across them, and tighter genetic correlations in high‐risk than in low‐risk treatments. We identified genetic variation in plasticity, with genetic correlations between boldness, sociality, and antipredator morphology, as expected, being tighter within treatments than across them, for both of two populations. By contrast, genetic correlations did not tighten with exposure to risk. Tighter phenotypic correlations in wild stickleback may thus arise because predators induce correlational selection on environmental components of these traits, or because predators tighten residual correlations by causing environmental heterogeneity that is controlled in the laboratory. Our study places phenotypic integration firmly into an ecological context.     

Environmental effects on the structure of the G‐matrix

Genetic correlations between traits determine the multivariate response to selection in the short term, and thereby play a causal role in evolutionary change. Although individual studies have documented environmentally induced changes in genetic correlations, the nature and extent of environmental effects on multivariate genetic architecture across species and environments remain largely uncharacterized. We reviewed the literature for estimates of the genetic variance–covariance ( G ) matrix in multiple environments, and compared differences in G between environments to the divergence in G between conspecific populations (measured in a common garden). We found that the predicted evolutionary trajectory differed as strongly between environments as it did between populations. Between‐environment differences in the underlying structure of G (total genetic variance and the relative magnitude and orientation of genetic correlations) were equal to or greater than between‐population differences. Neither environmental novelty, nor the difference in mean phenotype predicted these differences in G . Our results suggest that environmental effects on multivariate genetic architecture may be comparable to the divergence that accumulates over dozens or hundreds of generations between populations. We outline avenues of future research to address the limitations of existing data and characterize the extent to which lability in genetic correlations shapes evolution in changing environments.     

Phenotypic similarity and the evolutionary significance of countergradient variation

Countergradient variation is a geographical pattern of genotypes (with respect to environments) in which genetic influences on a trait oppose environmental influences, thereby minimizing phenotypic change along the gradient. Phenotypic similarity across changing environments ought to be of intense interest because it belies considerable genotypic change. When it occurs in characters that are positively associated with fitness, countergradient variation conflicts with the hypothesis that local adaptation to one environment trades off against performance in another environment. Cases of countergradient variation therefore offer unique insight into the mechanisms that produce and maintain phenotypic similarity and/or differences along environmental gradients.     

Environmentally induced changes in correlated responses to selection reveal variable pleiotropy across a complex genetic network

Selection in novel environments can lead to a coordinated evolutionary response across a suite of characters. Environmental conditions can also potentially induce changes in the genetic architecture of complex traits, which in turn could alter the pattern of the multivariate response to selection. We describe a factorial selection experiment using the nematode Caenorhabditis remanei in which two different stress‐related phenotypes (heat and oxidative stress resistance) were selected under three different environmental conditions. The pattern of covariation in the evolutionary response between phenotypes or across environments differed depending on the environment in which selection occurred, including asymmetrical responses to selection in some cases. These results indicate that variation in pleiotropy across the stress response network is highly sensitive to the external environment. Our findings highlight the complexity of the interaction between genes and environment that influences the ability of organisms to acclimate to novel environments. They also make clear the need to identify the underlying genetic basis of genetic correlations in order understand how patterns of pleiotropy are distributed across complex genetic networks.     

Does personality in small rodents vary depending on population density?

Personality means an individual's unique way of behaving and reacting to the environment. It is a stable and heritable trait, which is expressed consistently in different situations. The aim of our study was to develop novel tests to depict the personality structure of the bank vole Myodes glareolus, and to determine if the phase of the population cycle, i.e. population density, affects personality. We focused on some central aspects of bank vole behaviour: mobility, risk taking, exploratory behaviour, dominance, and aggressive behaviour towards pups. These behaviours were chosen because they directly affect bank vole survival or fitness or are classified as important factors of personality in other species. In total, 192 males from different populations went through four behavioural tests, in which 20 variables were measured. The tests were repeated after 3 weeks, which verified that all traits were stable, i.e. repeatable between trials. Three personality compounds emerged, named extroversion, novelty seeking and infanticide. Extroversion included dominance and mobility, while novelty seeking consisted of risk taking and exploration. Infanticide encompassed all indices measuring harmful behaviour towards pups. Mobility and dominance were connected, possibly because both seem to depend on condition. Time spent in captivity increased extroversion, which may be explained by good food, stable conditions and acclimation to strong social cues. Novelty seeking was connected to repeatability which could mean that novelty avoiding individuals adjust their behaviour to match new environments. Population density affected the infanticide trait but not novelty seeking or extroversion.     

Does education mediate the relationship between IQ and age of first birth? A behavioural genetic analysis

This study presents a multivariate behavioural genetic analysis of the relationship between education, intelligence and age of first birth. Analyses investigated the mediational role of education in explaining the relationship between intelligence and age of first birth at both the phenotypic and behavioural genetic level. The data come from the National Longitudinal Survey of Youth (NLSY), a nationally representative survey that included genetically informative full- and half-sibling pairs (n = 1423 pairs). Respondents were aged 14 to 22 when contacted in 1979. Heritability estimates were 0.32, 0.50 and 0.06 for IQ, education and age of first birth, respectively. Shared environment estimates were 0.35, 0.23 and 0.20 respectively. Common genetic and shared environmental factors were substantial in explaining the relationship between intelligence and education, and also education and age of first birth. Education partially mediated the relationship between intelligence and age of first birth only in the phenotypic analyses. After considering the genetic and shared environmental factors that influence all three variables, evidence for mediation was less convincing. This pattern of results suggests that the apparent mediational role of education at the phenotypic level is in fact the result of underlying genetic and shared environmental influences that affect education, IQ and age of first birth in common.     

The impact of plasticity and maternal effect on the evolution of leaf resin production in Diplacus aurantiacus

Our previous quantitative genetic study of leaf resin production in Diplacus aurantiacus revealed large environmental and maternal effects on variation in resin production, which suggests the possibility of a genotype×environment interaction for this trait when plants grow in heterogeneous environments. Our objectives in this study were to observe the genetic variation in plasticity of resin production under field and chamber conditions, compare phenotypic correlations of resin content with growth traits under these two environmental conditions, and distinguish the possible basis of the maternal effect on resin production using parents and half-sib progeny. A significant genotype×environment interaction (P<0.0001) in leaf resin production was found, which suggests a potential for the evolution of plasticity of these secondary metabolites under heterogeneous environments. The phenotypic correlation between resin content and growth rate also exhibited plasticity. In addition, the resin content of dam half-sib families grown in the chamber had a closer relationship with their maternal parents in the field (r=0.65, P=0.059) than in the chamber (r=0.39, P=0.34), suggesting an environmentally based maternal effect on the secondary chemicals. We suggest that the maternal environmental effect may act as a contributor to plasticity of resin production and, while it may not diminish the appearance of the genotype×environment interaction, the heritable variation of plasticity of resin production may be confounded.     

Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini

We studied the potential for response to selection in typical physiological-thermoregulatory traits of mammals such as maximum metabolic rate (MMR), nonshivering thermogenesis (NST) and basal metabolic rate (BMR) on cold-acclimated animals. We used an animal model approach to estimate both narrow-sense heritabilities (h2) and genetic correlations between physiological and growth-related traits. Univariate analyses showed that MMR presented high, significant heritability (h2 = 0.69 +/- 0.35, asymptotic standard error), suggesting the potential for microevolution in this variable. However, NST and BMR presented low, nonsignificant h2, and NST showed large maternal/common environmental/nonadditive effects (c2 = 0.34 +/- 0.17). Heritabilities were large and significant (h2 > 0.5) for all growth-related traits (birth mass, growth rate, weaning mass). The only significant genetic correlations we found between a physiological trait and a growth-related trait was between NST and birth mass (r = -0.74; P < 0.05). Overall, these results suggest that additive genetic variance is present in several bioenergetic traits, and that genetic correlations could be present between those different kinds of traits.     

THE EFFECT OF A VARIABLE ENVIRONMENT ON THE GENETIC CORRELATION STRUCTURE IN A FIELD CRICKET

The evolutionary trajectory of a trait depends not only on the presence of genetic variation, but also on the pattern of genetic correlations (r_g) among traits. Genetic correlations are most easily measured under homogeneous, controlled laboratory conditions, whereas natural populations typically experience a higher degree of environmental variability. The effect of environmental variability on genetic correlations in the cricket, Gryllus pennsylvanicus, was studied by measuring genetic correlations within and between two environments differing in levels of environmental heterogeneity. Within-environment r_g among morphological traits measured in the homogeneous laboratory environment were found to be reliable predictors of r_g measured in the experimental field environment. Laboratory measures of r_g involving life-history traits, though, were not found to reflect the same correlations measured in the heterogeneous environment. A significant negative genetic correlation between fecundity and developmental time was found in the field environment, yet was not detectable when measured in the laboratory. Phenotypic correlations may be obtained much more easily than genetic correlations, but their usefulness in evolutionary inference depends on the pattern of similarity between the two correlations. A comparison of genetic and phenotypic correlations revealed a close match between the two measures for morphological traits, but revealed only broad similarities when considering life-history traits. Male-female genetic correlations between morphological traits were high (all r_g > 0.73) and were consistently higher in the field environment than in the laboratory. The genetic correlations between the sexes in developmental time followed the same trend, but the male-female genetic correlation of gonad weights was low in both environments. Across-environment correlations were found to be strong for morphological traits and for gonad weight, whereas the genetic expression of developmental time was found to be dependent on the environment in which the crickets were raised.     

Ghrelin Influences Novelty Seeking Behavior in Rodents and Men

Recent discoveries indicate an important role for ghrelin in drug and alcohol reward and an ability of ghrelin to regulate mesolimbic dopamine activity. The role of dopamine in novelty seeking, and the association between this trait and drug and alcohol abuse, led us to hypothesize that ghrelin may influence novelty seeking behavior. To test this possibility we applied several complementary rodent models of novelty seeking behavior, i.e. inescapable novelty-induced locomotor activity (NILA), novelty-induced place preference and novel object exploration, in rats subjected to acute ghrelin receptor (growth hormone secretagogue receptor; GHSR) stimulation or blockade. Furthermore we assessed the possible association between polymorphisms in the genes encoding ghrelin and GHSR and novelty seeking behavior in humans. The rodent studies indicate an important role for ghrelin in a wide range of novelty seeking behaviors. Ghrelin-injected rats exhibited a higher preference for a novel environment and increased novel object exploration. Conversely, those with GHSR blockade drastically reduced their preference for a novel environment and displayed decreased NILA. Importantly, the mesolimbic ventral tegmental area selective GHSR blockade was sufficient to reduce the NILA response indicating that the mesolimbic GHSRs might play an important role in the observed novelty responses. Moreover, in untreated animals, a striking positive correlation between NILA and sucrose reward behavior was detected. Two GHSR single nucleotide polymorphisms (SNPs), rs2948694 and rs495225, were significantly associated with the personality trait novelty seeking, as assessed using the Temperament and Character Inventory (TCI), in human subjects. This study provides the first evidence for a role of ghrelin in novelty seeking behavior in animals and humans, and also points to an association between food reward and novelty seeking in rodents.     

Protein deprivation facilitates the independent evolution of behavior and morphology

Ecological conditions such as nutrition can change genetic covariances between traits and accelerate or slow down trait evolution. As adaptive trait correlations can become maladaptive following rapid environmental change, poor or stressful environments are expected to weaken genetic covariances, thereby increasing the opportunity for independent evolution of traits. Here, we demonstrate the differences in genetic covariance among multiple behavioral and morphological traits (exploration, aggression, and body weight) between southern field crickets (Gryllus bimaculatus) raised in favorable (free‐choice) versus stressful (protein‐deprived) nutritional environments. We also quantify the extent to which differences in genetic covariance structures contribute to the potential for the independent evolution of these traits. We demonstrate that protein‐deprived environments tend to increase the potential for traits to evolve independently, which is caused by genetic covariances that are significantly weaker for crickets raised on protein‐deprived versus free‐choice diets. The weakening effects of stressful environments on genetic covariances tended to be stronger in males than in females. The weakening of the genetic covariance between traits under stressful nutritional environments was expected to facilitate the opportunity for adaptive evolution across generations. Therefore, the multivariate gene‐by‐environment interactions revealed here may facilitate behavioral and morphological adaptations to rapid environmental change.