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.     

Effects of the demographic transition on the genetic variances and covariances of human life‐history traits

The recent demographic transitions to lower mortality and fertility rates in most human societies have led to changes and even quick reversals in phenotypic selection pressures. This can only result in evolutionary change if the affected traits are heritable, but changes in environmental conditions may also lead to subsequent changes in the genetic variance and covariance (the G matrix) of traits. It currently remains unclear if there have been concomitant changes in the G matrix of life‐history traits following the demographic transition. Using 300 years of genealogical data from Finland, we found that four key life‐history traits were heritable both before and after the demographic transition. The estimated heritabilities allow a quantifiable genetic response to selection during both time periods, thus facilitating continued evolutionary change. Further, the G matrices remained largely stable but revealed a trend for an increased additive genetic variance and thus evolutionary potential of the population after the transition. Our results demonstrate the validity of predictions of evolutionary change in human populations even after the recent dramatic environmental change, and facilitate predictions of how our biology interacts with changing environments, with implications for global public health and demography.     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

A large‐scale latitudinal pattern of life‐history traits in a strictly univoltine damselfly

1. Variation in thermal conditions and season length along latitudinal gradients affect body size‐related traits over different life stages. Selection is expected to optimise these size traits in response to the costs and benefits. 2. Egg, hatchling, larval and adult size in males and females were estimated along a latitudinal gradient of 2730 km across Europe in the univoltine damselfly Lestes sponsa, using a combination of field‐collection and laboratory‐rearing experiments. In the laboratory, individuals were grown in temperatures and photoperiod simulating those at the latitude of origin, and in common‐garden conditions. 3. The size of adults sampled in nature was negatively correlated with latitude. In all populations the females were larger than the males. Results from simulated and common‐garden rearing experiments supported this pattern of size difference across latitudes and between sexes, suggesting a genetic component for the latitudinal size trend and female‐biased size dimorphism. In contrast, hatchling size showed a positive relationship with latitude, but egg size, although differing between latitudes, showed no such relationship. 4. The results support a converse Bergmann cline, i.e. a negative body size cline towards the north. This negative cline in body size is probably driven by progressively stronger seasonal time and temperature constraints towards the higher latitudes and by the obligate univoltine life cycle of L. sponsa. As egg size showed no relationship with latitude, other environmental factors besides temperature, such as desiccation risk, probably affect this trait.     

The role of genetic constraints on the diversification of Iberian taxa of the genus Aquilegia (Ranunculaceae)

The microevolutionary process of adaptive phenotypic differentiation of quantitative traits between populations or closely‐related taxa depends on the response of populations to the action of natural selection. However, this response can be constrained by the structure of the matrix of additive genetic variance and covariance between traits in each population ( G matrix). In the present study, we obtained additive genetic variance and narrow sense heritability for 25 floral and vegetative traits of three subspecies of Aquilegia vulgaris, and one subspecies of Aquilegia pyrenaica through a common garden crossing experiment. For two vegetative and one floral trait, we also obtained the G matrix and genetic correlations between traits in each subspecies. The amount of genetic variation available in wild populations is not responsible for the larger differentiation of vegetative than floral traits found in this group of columbines. However, the low heritability of some traits constrained their evolution because phenotypic variability among taxa was larger for traits with larger heritability. We confirmed that the process of diversification of the studied taxa involved shifts in the G matrix, mainly determined by changes in the genetic covariance between floral and vegetative traits, probably caused by linkage disequilibrium in narrow endemic taxa. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 252–261.     

Weak impact of fine‐scale landscape heterogeneity on evolutionary potential in Arabidopsis lyrata

Microhabitat heterogeneity can lead to fine‐scale local adaptation when gene flow is restricted, which may be important for the maintenance of genetic variation within populations. This study tested whether microhabitat heterogeneity was associated with trait differences in a population of Arabidopsis lyrata and studied its impact on the genetic variance–covariance (G) matrix. Maternal seed families were collected from dune tops and bottoms, two microhabitats known to vary significantly in water availability. In a common garden experiment, replicate individuals per family were raised under wet and dry conditions, and physiological, morphological and life‐history traits were assessed. Plants from the two microenvironments differed in their response to treatment in two performance components, in stomata density and most strongly in flowering time. Under wet conditions, plants originating from dune bottoms flowered 4 weeks earlier than those from dune tops. Only one of three G‐matrix comparisons revealed that habitat heterogeneity and evolutionary potential were positively linked. The number of independent trait dimensions was larger in the entire population than within subpopulations separated by microhabitat under wet conditions. However, the size of the G‐matrix was no larger in the entire population than within subpopulations separated by microhabitat, and trait correlation structure between microhabitats and treatments was not significantly different. These results indicate that fine‐scale habitat heterogeneity likely led to local adaptation, which weakly affected levels of across‐trait genetic variation.     

Two experimental designs generate contrasting patterns of behavioral differentiation along a latitudinal gradient in Lestes sponsa—Common‐garden not so common after all?

Understanding why and how behavioral profiles differ across latitudes can help predict behavioral responses to environmental change. The first response to environmental change that an organism exhibits is commonly a behavioral response. Change in one behavior usually results in shifts in other correlated behaviors, which may adaptively or maladaptively vary across environments and/or time. However, one important aspect that is often neglected when studying behavioral expressions among populations is if/how the experimental design might affect the results. This is unfortunate since animals often plastically modify their behavior to the environment, for example, rearing conditions. We studied behavioral traits and trait correlations in larvae of a univoltine damselfly, Lestes sponsa, along its latitudinal distribution, spreading over 3,300 km. We compared behavioral profiles among larvae grown in two conditions: (a) native temperatures and photoperiods or (b) averaged constant temperatures and photoperiods (common‐garden). We hypothesized latitudinal differences in behavioral traits regardless of the conditions in which larvae were grown, with northern populations expressing higher activity, boldness, and foraging efficiency. When grown in native conditions, northern larvae were bolder, more active and more effective in prey capture than central and low latitude populations, respectively, as well as showed the strongest behavioral correlations. In contrast, larvae reared in common‐garden conditions showed no differences between regions in both individual traits and trait correlations. The results suggest different selective pressures acting on the studied traits across populations, with environment as a central determinant of the observed trait values. Common‐garden designed experiments may evoke population‐dependent levels of plastic response to the artificial conditions and, hence, generate results that lack ecological relevance when studying multi‐population differences in behavior.     

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.     

Adaptive and non‐adaptive evolution of trait means and genetic trait correlations for herbivory resistance and performance in an invasive plant

The EICA‐hypothesis predicts that invading plants adapt to their novel environment by evolving increased performance and reduced resistance in response to the release from natural enemies, and assumes a resource allocation tradeoff among both trait groups as mechanistic basis of this evolutionary change. Using the plant Silene latifolia as a study system, we tested these predictions by investigating whether 1) invasive populations evolved lower resistance and higher performance, 2) this evolutionary change is indeed adaptive, and 3) there is a negative genetic correlation between performance and resistance (i.e. a tradeoff) in native and introduced individuals. Moreover, we sampled eight native and eight invasive populations and determined their population co‐ancestry based on neutral SSR‐markers. We performed controlled crossings to produce five sib‐groups per population and exposed them to increased and reduced levels of enemy attack in a full‐factorial experiment to estimate performance and resistance. With these data, we performed trait‐by‐trait comparisons between ranges with ‘animal models’ that account for population co‐ancestry to quantify the amount of variance in traits explained by non‐adaptive versus adaptive evolution. Moreover, we tested for genetic correlations among performance and resistance traits within sib‐groups. We found significant reductions in resistance and increases in performance in invasive versus native populations, which could largely be attributed to adaptive evolution. While we detected a non‐significant trend towards negative genetic performance × resistance correlations in native populations, invasive populations exhibited both significant and non‐significant positive correlations. In summary, these results do not support a shift of performance and resistance trait values along a tradeoff line in response to enemy release, as predicted by EICA. They rather suggest that the independent evolution of both traits is not constrained by a tradeoff, and that various selective agents (including resource availability) interact in shaping both traits and in weakening negative genetic correlations in the invaded habitat.     

Environmentally triggered variability in the genetic variance–covariance of herbivory resistance of an exotic plant Solidago altissima

The variability in the genetic variance–covariance (G‐matrix) in plant resistance and its role in the evolution of invasive plants have been long overlooked. We conducted an additional analysis of the data of a reciprocal transplant experiment with tall goldenrod, Solidago altissima, in multiple garden sites within its native range (USA) and introduced range (Japan). We explored the differences in G‐matrix of resistance to two types of foliar herbivores: (a) a lace bug that is native to the USA and recently introduced to Japan, (b) and other herbivorous insects in response to plant origins and environments. A negative genetic covariance was found between plant resistances to lace bugs and other herbivorous insects, in all combinations of garden locations and plant origins except for US plants planted in US gardens. The G‐matrix of the resistance indices did not differ between US and Japanese plants either in US or Japanese gardens, while it differed between US and Japanese gardens in both US and Japanese plants. Our results suggested that the G‐matrix of the plant resistance may have changed in response to novel environmental differences including herbivore communities and/or other biotic and abiotic factors in the introduced range. This may have revealed a hidden trade‐off between resistances, masked by the environmental factors in the origin range. These results suggest that the stability of the genetic covariance during invasion, and the environmentally triggered variability in the G‐matrices of plant resistance may help to protect the plant against multiple herbivore species without changing its genetic architecture and that this may lead to a rapid adaptation of resistance in exotic plants. Local environments of the plant also have a critical effect on plant resistance and should be considered in order to understand trait evolution in exotic plants.     

Selection on life‐history traits and genetic population divergence in rotifers

A combination of founder effects and local adaptation – the Monopolization hypothesis – has been proposed to reconcile the strong population differentiation of zooplankton dwelling in ponds and lakes and their high dispersal abilities. The role genetic drift plays in genetic differentiation of zooplankton is well documented, but the impact of natural selection has received less attention. Here, we compare differentiation in neutral genetic markers (F_ST) and in quantitative traits (Q_ST) in six natural populations of the rotifer Brachionus plicatilis to assess the importance of natural selection in explaining genetic differentiation of life‐history traits. Five life‐history traits were measured in four temperature × salinity combinations in common‐garden experiments. Population differentiation for neutral genetic markers – 11 microsatellite loci – was very high (F_ST = 0.482). Differentiation in life‐history traits was higher in traits related to sexual reproduction than in those related to asexual reproduction. Q_ST values for diapausing egg production (a trait related to sexual reproduction) were higher than their corresponding F_ST in some pairs of populations. Our results indicate the importance of divergent natural selection in these populations and suggest local adaptation to the unpredictability of B. plicatilis habitats.     

Characterizing the evolution of genetic variance using genetic covariance tensors

Determining how genetic variance changes under selection in natural populations has proved to be a very resilient problem in evolutionary genetics. In the same way that understanding the availability of genetic variance within populations requires the simultaneous consideration of genetic variance in sets of functionally related traits, determining how genetic variance changes under selection in natural populations will require ascertaining how genetic variance–covariance (G) matrices evolve. Here, we develop a geometric framework using higher-order tensors, which enables the empirical characterization of how G matrices have diverged among populations. We then show how divergence among populations in genetic covariance structure can then be associated with divergence in selection acting on those traits using key equations from evolutionary theory. Using estimates of G matrices of eight male sexually selected traits from nine geographical populations of Drosophila serrata, we show that much of the divergence in genetic variance occurred in a single trait combination, a conclusion that could not have been reached by examining variation among the individual elements of the nine G matrices. Divergence in G was primarily in the direction of the major axes of genetic variance within populations, suggesting that genetic drift may be a major cause of divergence in genetic variance among these populations.     

Among‐population variation and correlations in sexually dimorphic traits of Silene latifolia

Abstract The degree of sexual dimorphism in a trait may be determined directly by disruptive selection, as well as by correlations with other traits under selection. We grew seeds from nine populations of the dioecious plant Silene latifolia in a common‐garden experiment to determine whether phenotypic variation and correlations existed for floral, leaf and resource allocation traits, and whether this variation had a genetic component. We also determined the traits which were sexually dimorphic, the degree of dimorphism, and whether it varied among populations. Seven traits exhibited among‐population variation and sexual dimorphism. Variation in the degree of dimorphism occurred only for two traits, suggesting that dimorphism may be evolving more slowly than trait means. Males had more, smaller flowers, shorter leaves, and allocated less of their total biomass to stems and more to leaves than females. Flower production was the most sexually dimorphic trait and was correlated with all measured traits. Most traits exhibited significant correlations between the sexes. The pattern of correlations and the degree of sexual dimorphism among traits lead us to suggest that intrasexual selection for an exaggerated floral display in males has indirectly led to sexual dimorphism in a host of other traits.     

Genetic variation in flowering phenology and avoidance of seed predation in native populations of Ulex europaeus

The genetic variation in flowering phenology may be an important component of a species’ capacity to colonize new environments. In native populations of the invasive species Ulex europaeus, flowering phenology has been shown to be bimodal and related to seed predation. The aim of the present study was to determine if this bimodality has a genetic basis, and to investigate whether the polymorphism in flowering phenology is genetically linked to seed predation, pod production and growth patterns. We set up an experiment raising maternal families in a common garden. Based on mixed analyses of variance and correlations among maternal family means, we found genetic differences between the two main flowering types and confirmed that they reduced seed predation in two different ways: escape in time or predator satiation. We suggest that this polymorphism in strategy may facilitate maintain high genetic diversity for flowering phenology and related life‐history traits in native populations of this species, hence providing high evolutionary potential for these traits in invaded areas.     

Phenotypic constraints and community structure: Linking trade‐offs within and among species

Trade‐offs are central to many topics in biology, from the evolution of life histories to ecological mechanisms of species coexistence. Trade‐offs observed among species may reflect pervasive constraints on phenotypes that are achievable given biophysical and resource limitations. If so, then among‐species trade‐offs should be consistent with trade‐offs within species. Alternatively, trait variation among co‐occurring species may reflect historical contingencies during community assembly rather than within‐species constraints. Here, we test whether a key trade‐off between relative growth rate (RGR) and water‐use efficiency (WUE) among Sonoran Desert winter annual plants is apparent within four species representing different strategies in the system. We grew progeny of maternal families from multiple populations in a greenhouse common garden. One species, Pectocarya recurvata, displayed the expected RGR–WUE trade‐off among families within populations. For other species, although RGR and WUE often varied clinally among populations, among‐family variation within populations was lacking, implicating a role for past selection on these traits. Our results suggest that a combination of limited genetic variation in single traits and negative trait correlations could pose constraints on the evolution of a high‐RGR and high‐WUE phenotype within species, providing a microevolutionary explanation for phenotypes that influence community‐level patterns of abundance and coexistence.     

Population differences in early life‐history traits in grayling

In this paper we test population differences in early life‐history traits in three grayling Thymallus thymallus populations. The grayling shared ancestors some 80–90 years ago. We performed common‐garden experiments at three temperatures (mimicking population‐specific summer temperatures), and measured survival and growth rates during early development. We found significant additive genetic variance in size (length and yolk‐sac volume) measured at hatching, swim‐up and termination of the experiment, and significantly different reaction norms for growth rate and survival during the period of first feeding. In general, each population did best at the temperature experienced in nature. These differences in early life‐history traits suggest that natural selection has resulted in local adaptation in a time period of 13–18 generations.     

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.     

Invasive plants and enemy release: evolution of trait means and trait correlations in Ulex europaeus

Several hypotheses that attempt to explain invasive processes are based on the fact that plants have been introduced without their natural enemies. Among them, the EICA (Evolution of Increased Competitive Ability) hypothesis is the most influential. It states that, due to enemy release, exotic plants evolve a shift in resource allocation from defence to reproduction or growth. In the native range of the invasive species Ulex europaeus, traits involved in reproduction and growth have been shown to be highly variable and genetically correlated. Thus, in order to explore the joint evolution of life history traits and susceptibility to seed predation in this species, we investigated changes in both trait means and trait correlations. To do so, we compared plants from native and invaded regions grown in a common garden. According to the expectations of the EICA hypothesis, we observed an increase in seedling height. However, there was little change in other trait means. By contrast, correlations exhibited a clear pattern: the correlations between life history traits and infestation rate by seed predators were always weaker in the invaded range than in the native range. In U. europaeus, the role of enemy release in shaping life history traits thus appeared to imply trait correlations rather than trait means. In the invaded regions studied, the correlations involving infestation rates and key life history traits such as flowering phenology, growth and pod density were reduced, enabling more independent evolution of these key traits and potentially facilitating local adaptation to a wide range of environments. These results led us to hypothesise that a relaxation of genetic correlations may be implied in the expansion of invasive species.     

Genotype‐by‐environment interactions underlie the expression of pre‐ and post‐copulatory sexually selected traits in guppies

The role that genotype‐by‐environment interactions (GEIs) play in sexual selection has only recently attracted the attention of evolutionary biologists. Yet GEIs can have profound evolutionary implications by compromising the honesty of sexual signals, maintaining high levels of genetic variance underlying their expression and altering the patterns of genetic covariance among fitness traits. In this study, we test for GEIs in a highly sexually dimorphic freshwater fish, the guppy Poecilia reticulata. We conducted an experimental quantitative genetic study in which male offspring arising from a paternal half‐sibling breeding design were assigned to differing nutritional ‘environments’ (either high or low feed levels). We then determined whether the manipulation of diet quantity influenced levels of additive genetic variance and covariance for several highly variable and condition‐dependent pre‐ and post‐copulatory sexual traits. In accordance with previous work, we found that dietary limitation had strong phenotypic effects on numerous pre‐ and post‐copulatory sexual traits. We also report evidence for significant GEI for several of these traits, which in some cases (area of iridescence and sperm velocity) reflected a change in the rank order of genotypes across different nutritional environments (i.e. ecological crossover). Furthermore, we show that genetic correlations vary significantly between nutritional environments. Notably, a highly significant negative genetic correlation between iridescent coloration and sperm viability in the high food treatment broke down under dietary restriction. Taken together, these findings are likely to have important evolutionary implications for guppies; ecological crossover may influence sexual signal reliability in unstable (nutritional) environments and contribute towards the extreme levels of polymorphism in sexual traits typically reported for this species. Furthermore, the presence of environment‐specific genetic covariance suggests that trade‐offs measured in one environment may not be indicative of genetic constraints in others.     

Heritability and evolvability of fitness and nonfitness traits: Lessons from livestock

Data from natural populations have suggested a disconnection between trait heritability (variance standardized additive genetic variance, V_A) and evolvability (mean standardized V_A) and emphasized the importance of environmental variation as a determinant of trait heritability but not evolvability. However, these inferences are based on heterogeneous and often small datasets across species from different environments. We surveyed the relationship between evolvability and heritability in >100 traits in farmed cattle, taking advantage of large sample sizes and consistent genetic approaches. Heritability and evolvability estimates were positively correlated (r = 0.37/0.54 on untransformed/log scales) reflecting a substantial impact of V_A on both measures. Furthermore, heritabilities and residual variances were uncorrelated. The differences between this and previously described patterns may reflect lower environmental variation experienced in farmed systems, but also low and heterogeneous quality of data from natural populations. Similar to studies on wild populations, heritabilities for life‐history and behavioral traits were lower than for other traits. Traits having extremely low heritabilities and evolvabilities (17% of the studied traits) were almost exclusively life‐history or behavioral traits, suggesting that evolutionary constraints stemming from lack of genetic variability are likely to be most common for classical “fitness” (cf. life‐history) rather than for “nonfitness” (cf. morphological) traits.