Strong ecological but weak evolutionary effects of elevated CO2 on a recombinant inbred population of Arabidopsis thaliana

Increases in atmospheric CO2 concentration have an impact on plant communities by influencing plant growth and morphology, species interactions, and ecosystem processes. These ecological effects may be accompanied by evolutionary change if elevated CO2 (eCO2) alters patterns of natural selection or expression of genetic variation. Here, a statistically powerful quantitative genetic experiment and manipulations of CO2 concentrations in a field setting were used to investigate how eCO2 impacts patterns of selection on ecologically important traits in Arabidopsis thaliana; heritabilities, which influence the rate of response to selection; and genetic covariances between traits, which may constrain responses to selection. CO2 had strong phenotypic effects; plants grown in eCO2 were taller and produced more biomass and fruits. Also, significant directional selection was observed on many traits and significant genetic variation was observed for all traits. However, no evolutionary effect of eCO2 was detected; patterns of selection, heritabilities and genetic correlations corresponded closely in ambient and elevated CO2 environments. The data suggest that patterns of natural selection and the quantitative genetic parameters of this A. thaliana population are robust to increases in CO2 concentration and that responses to eCO2 will be primarily ecological.     

Does natural selection promote population divergence? A comparative analysis of population structure using amplified fragment length polymorphism markers and quantitative traits

Divergent natural selection is considered an important force in plant evolution leading to phenotypic differentiation between populations exploiting different environments. Extending an earlier greenhouse study of population differentiation in the selfing annual plant Senecio vulgaris, we estimated the degree of population divergence in several quantitative traits related to growth and life history and compared these estimates with those based on presumably neutral molecular markers (amplified fragment length polymorphisms; AFLPs). This approach allowed us to disentangle the effects of divergent selection from that of other evolutionary forces (e.g. genetic drift). Five populations were examined from each of two habitat types (ruderal and agricultural habitats). We found a high proportion of total genetic variance to be among populations, both for AFLP markers (phiST = 0.49) and for quantitative traits (range of QST: 0.26-0.77). There was a strong correlation between molecular and quantitative genetic differentiation between pairs of populations (Mantel's r = 0.59). However, estimates of population differentiation in several quantitative traits exceeded the neutral expectation (estimated from AFLP data), suggesting that divergent selection contributed to phenotypic differentiation, especially between populations from ruderal and agricultural habitats. Estimates of within-population variation in AFLP markers and quantitative genetic were poorly correlated, indicating that molecular marker data may be of limited value to predict the evolutionary potential of populations of S. vulgaris.     

Divergent selection along climatic gradients in a rare central European endemic species,Saxifraga sponhemica

Background and Aims The effects of habitat fragmentation on quantitative genetic variation in plant populations are still poorly known. Saxifraga sponhemica is a rare endemic of Central Europe with a disjunct distribution, and a stable and specialized habitat of treeless screes and cliffs. This study therefore used S. sponhemica as a model species to compare quantitative and molecular variation in order to explore (1) the relative importance of drift and selection in shaping the distribution of quantitative genetic variation along climatic gradients; (2) the relationship between plant fitness, quantitative genetic variation, molecular genetic variation and population size; and (3) the relationship between the differentiation of a trait among populations and its evolvability.Methods Genetic variation within and among 22 populations from the whole distribution area of S. sponhemica was studied using RAPD (random amplified polymorphic DNA) markers, and climatic variables were obtained for each site. Seeds were collected from each population and germinated, and seedlings were transplanted into a common garden for determination of variation in plant traits.Key Results In contrast to previous results from rare plant species, strong evidence was found for divergent selection. Most population trait means of S. sponhemica were significantly related to climate gradients, indicating adaptation. Quantitative genetic differentiation increased with geographical distance, even when neutral molecular divergence was controlled for, and Q_ST exceeded F_ST for some traits. The evolvability of traits was negatively correlated with the degree of differentiation among populations (Q_ST), i.e. traits under strong selection showed little genetic variation within populations. The evolutionary potential of a population was not related to its size, the performance of the population or its neutral genetic diversity. However, performance in the common garden was lower for plants from populations with reduced molecular genetic variation, suggesting inbreeding depression due to genetic erosion.Conclusions The findings suggest that studies of molecular and quantitative genetic variation may provide complementary insights important for the conservation of rare species. The strong differentiation of quantitative traits among populations shows that selection can be an important force for structuring variation in evolutionarily important traits even for rare endemic species restricted to very specific habitats.     

Heritability,covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment

This study explored genetic variation and co‐variation in multiple functional plant traits. Our goal was to characterize selection, heritabilities and genetic correlations among different types of traits to gain insight into the evolutionary ecology of plant populations and their interactions with insect herbivores. In a field experiment, we detected significant heritable variation for each of 24 traits of Oenothera biennis and extensive genetic covariance among traits. Traits with diverse functions formed several distinct groups that exhibited positive genetic covariation with each other. Genetic variation in life‐history traits and secondary chemistry together explained a large proportion of variation in herbivory (r² = 0.73). At the same time, selection acted on lifetime biomass, life‐history traits and two secondary compounds of O. biennis, explaining over 95% of the variation in relative fitness among genotypes. The combination of genetic covariances and directional selection acting on multiple traits suggests that adaptive evolution of particular traits is constrained, and that correlated evolution of groups of traits will occur, which is expected to drive the evolution of increased herbivore susceptibility. As a whole, our study indicates that an examination of genetic variation and covariation among many different types of traits can provide greater insight into the evolutionary ecology of plant populations and plant–herbivore interactions.     

Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology

BACKGROUND: The model plant Arabidopsis thaliana (Arabidopsis) shows a wide range of genetic and trait variation among wild accessions. Because of its unparalleled biological and genomic resources, the potential of Arabidopsis for molecular genetic analysis of this natural variation has increased dramatically in recent years. SCOPE: Advanced genomics has accelerated molecular phylogenetic analysis and gene identification by quantitative trait loci (QTL) mapping and/or association mapping in Arabidopsis. In particular, QTL mapping utilizing natural accessions is now becoming a major strategy of gene isolation, offering an alternative to artificial mutant lines. Furthermore, the genomic information is used by researchers to uncover the signature of natural selection acting on the genes that contribute to phenotypic variation. The evolutionary significance of such genes has been evaluated in traits such as disease resistance and flowering time. However, although molecular hallmarks of selection have been found for the genes in question, a corresponding ecological scenario of adaptive evolution has been difficult to prove. Ecological strategies, including reciprocal transplant experiments and competition experiments, and utilizing near-isogenic lines of alleles of interest will be a powerful tool to measure the relative fitness of phenotypic and/or allelic variants. CONCLUSIONS: As the plant model organism, Arabidopsis provides a wealth of molecular background information for evolutionary genetics. Because genetic diversity between and within Arabidopsis populations is much higher than anticipated, combining this background information with ecological approaches might well establish Arabidopsis as a model organism for plant evolutionary ecology.     

The nature of quantittative genetic variation revisited: Lessons from Drosophila bristles

Most characters that distinguish one individual from another, like height or weight, vary continuously in populations. Continuous variation of these ‘quantitative’ traits is due to the simultaneous segregation of multiple quantitative trait loci (QTLs) as well as environmental influences. A major challenge in human medicine, animal and plant breeding and evolutionary genetics is to identify QTLs and determine their genetic properties. Studies of the classic quantitative traits, abdominal and sternopleural bristle numbers of Drosophila, have shown that: (1) many loci have small effects on bristle number, but a few have large effects and cause most of the genetic variation; (2) ‘candidate’ loci involved in bristle development often have large quantitative effects on bristle number; and (3) alleles at QTLs affecting bristle number have variable degrees of dominance, interact with each other, and affect other quantitative traits, including fitness. Lessons learned from this model system will be applicable to studies of the genetic basis of quantitative variation in other species.     

Genetic analysis of life-history constraint and evolution in a wild ungulate population

Trade-offs among life-history traits are central to evolutionary theory. In quantitative genetic terms, trade-offs may be manifested as negative genetic covariances relative to the direction of selection on phenotypic traits. Although the expression and selection of ecologically important phenotypic variation are fundamentally multivariate phenomena, the in situ quantification of genetic covariances is challenging. Even for life-history traits, where well-developed theory exists with which to relate phenotypic variation to fitness variation, little evidence exists from in situ studies that negative genetic covariances are an important aspect of the genetic architecture of life-history traits. In fact, the majority of reported estimates of genetic covariances among life-history traits are positive. Here we apply theory of the genetics and selection of life histories in organisms with complex life cycles to provide a framework for quantifying the contribution of multivariate genetically based relationships among traits to evolutionary constraint. We use a Bayesian framework to link pedigree-based inference of the genetic basis of variation in life-history traits to evolutionary demography theory regarding how life histories are selected. Our results suggest that genetic covariances may be acting to constrain the evolution of female life-history traits in a wild population of red deer Cervus elaphus: genetic covariances are estimated to reduce the rate of adaptation by about 40%, relative to predicted evolutionary change in the absence of genetic covariances. Furthermore, multivariate phenotypic (rather than genetic) relationships among female life-history traits do not reveal this constraint.     

PATTERNS OF GENETIC ARCHITECTURE FOR LIFE-HISTORY TRAITS AND MOLECULAR MARKERS IN A SUBDIVIDED SPECIES

Abstract Understanding the utility and limitations of molecular markers for predicting the evolutionary potential of natural populations is important for both evolutionary and conservation genetics. To address this issue, the distribution of genetic variation for quantitative traits and molecular markers is estimated within and among 14 permanent lake populations of Daphnia pulicaria representing two regional groups from Oregon. Estimates of population subdivision for molecular and quantitative traits are concordant, with Q _ST generally exceeding G _ST. There is no evidence that microsatellites loci are less informative about subdivision for quantitative traits than are allozyme loci. Character-specific comparison of Q _ST and G _ST support divergent selection pressures among populations for the majority of life-history traits in both coast and mountain regions. The level of within-population variation for molecular markers is uninformative as to the genetic variation maintained for quantitative traits. In D. pulicaria , regional differences in the frequency of sex may contribute to variation in the maintenance of expressed within-population quantitative-genetic variation without substantially impacting diversity at the genic level. These data are compared to an identical dataset for 17 populations of the temporary-pond species, D. pulex .     

Standing genetic variation in host preference for mutualist microbial symbionts

Many models of mutualisms show that mutualisms are unstable if hosts lack mechanisms enabling preferential associations with mutualistic symbiotic partners over exploitative partners. Despite the theoretical importance of mutualism-stabilizing mechanisms, we have little empirical evidence to infer their evolutionary dynamics in response to exploitation by non-beneficial partners. Using a model mutualism—the interaction between legumes and nitrogen-fixing soil symbionts—we tested for quantitative genetic variation in plant responses to mutualistic and exploitative symbiotic rhizobia in controlled greenhouse conditions. We found significant broad-sense heritability in a legume host''s preferential association with mutualistic over exploitative symbionts and selection to reduce frequency of associations with exploitative partners. We failed to detect evidence that selection will favour the loss of mutualism-stabilizing mechanisms in the absence of exploitation, as we found no evidence for a fitness cost to the host trait or indirect selection on genetically correlated traits. Our results show that genetic variation in the ability to preferentially reduce associations with an exploitative partner exists within mutualisms and is under selection, indicating that micro-evolutionary responses in mutualism-stabilizing traits in the face of rapidly evolving mutualistic and exploitative symbiotic bacteria can occur in natural host populations.     

Pattern and process: evidence for the evolution of photosynthetic traits in natural populations

The patterns of interspecific variation identified by comparative studies provide valuable hypotheses about the role of physiological traits in evolutionary adaptation. This review covers tests of these hypotheses for photosynthetic traits that have used a microevolutionary perspective to characterize physiological variation among and within populations. Studies of physiological differentiation among populations show that evolutionary divergence in photosynthetic traits is common within species, and has a pattern that supports many adaptive hypotheses. These among-population studies imply that selection has influenced photosynthetic traits in some way, but they are not designed to identify the traits targeted by selection or the environmental agents that cause selection. Analyses of genetic and phenotypic variation within populations address these questions. Studies that have quantified genetic variation within populations show that levels of heritable variation can be adequate for evolutionary change in photosynthetic traits. Other studies have measured phenotypic selection for these traits by analyzing how the variation within populations is correlated with fitness. This work has shown that selection for photosynthetic traits may often operate indirectly via correlations with other traits, and emphasizes the importance of viewing the phenotype as an integrated function of growth, morphology, life-history and physiology. We also outline some methodological problems that may be encountered for ecophysiological traits by these types of studies, provide some potential solutions, and discuss future directions for the field of plant evolutionary ecophysiology.     

To clone or not to clone plant QTLs: present and future challenges

Recent technical advancements and refinement of analytical methods have enabled the loci (quantitative trait loci, QTLs) responsible for the genetic control of quantitative traits to be dissected molecularly. To date, most plant QTLs have been cloned using a positional cloning approach following identification in experimental crosses. In some cases, an association between sequence variation at a candidate gene and a phenotype has been established by analysing existing genetic accessions. These strategies can be refined using appropriate genetic materials and the latest developments in genomics platforms. We foresee that although QTL analysis and cloning addressing naturally occurring genetic variation should shed light on mechanisms of plant adaptation, a greater emphasis on approaches relying on mutagenesis and candidate gene validation is likely to accelerate the pace of discovering the genes underlying QTLs.     

Genetic variation for growth,morphological, and physiological traits in a wild population of the Neotropical shade­tolerant rainforest tree <Emphasis Type="BoldItalic">Sextonia rubra</Emphasis> (Mez) van der Werff (Lauraceae)

Quantitative genetic diversity is a fundamental component of the interaction between natural populations and their environment. In breeding programmes, quantitative genetic studies on tropical trees have so far focused on fast-growing, light-demanding species, but no information exists on shade-tolerant, slow-growing species. For this study, 27 3-year-old open-pollinated families of the Neotropical shade-tolerant rainforest tree Sextonia rubra were measured in semicontrolled conditions for 20 morphological, growth, and photosynthesis traits; the effect of genetic relatedness, habitat of provenance, and mother tree status on seedling traits was analysed. Nine traits displayed significant genetic effects, while mother tree status and habitat effects were not significant (P > 0.05) for an y trait. Estimated heritability varied between 0.14 and 0.28, with growth-related traits having the highest values. Additive genetic variation correlated positively with nonheritable variation, suggesting that ecological–evolutionary factors increasing or decreasing additive genetic variance may also affect nonheritable variation in the same direction. Our results suggest that quantitative genetic variability should be taken into account in ecological studies on, and in the management of, natural tropical rainforests; further research is needed to investigate genetic × environment interactions, in particular from the point of view of the genetic response of shade-tolerant plant species to variations in light availability.     

Relaxation of herbivore‐mediated selection drives the evolution of genetic covariances between plant competitive and defense traits

Insect herbivores are important mediators of selection on traits that impact plant defense against herbivory and competitive ability. Although recent experiments demonstrate a central role for herbivory in driving rapid evolution of defense and competition‐mediating traits, whether and how herbivory shapes heritable variation in these traits remains poorly understood. Here, we evaluate the structure and evolutionary stability of the G matrix for plant metabolites that are involved in defense and allelopathy in the tall goldenrod, Solidago altissima. We show that G has evolutionarily diverged between experimentally replicated populations that evolved in the presence versus the absence of ambient herbivory, providing direct evidence for the evolution of G by natural selection. Specifically, evolution in an herbivore‐free habitat altered the orientation of G , revealing a negative genetic covariation between defense‐ and competition‐related metabolites that is typically masked in herbivore‐exposed populations. Our results may be explained by predictions of classical quantitative genetic theory, as well as the theory of acquisition‐allocation trade‐offs. The study provides compelling evidence that herbivory drives the evolution of plant genetic architecture.     

The complex genetic architecture of the metabolome

Discovering links between the genotype of an organism and its metabolite levels can increase our understanding of metabolism, its controls, and the indirect effects of metabolism on other quantitative traits. Recent technological advances in both DNA sequencing and metabolite profiling allow the use of broad-spectrum, untargeted metabolite profiling to generate phenotypic data for genome-wide association studies that investigate quantitative genetic control of metabolism within species. We conducted a genome-wide association study of natural variation in plant metabolism using the results of untargeted metabolite analyses performed on a collection of wild Arabidopsis thaliana accessions. Testing 327 metabolites against >200,000 single nucleotide polymorphisms identified numerous genotype-metabolite associations distributed non-randomly within the genome. These clusters of genotype-metabolite associations (hotspots) included regions of the A. thaliana genome previously identified as subject to recent strong positive selection (selective sweeps) and regions showing trans-linkage to these putative sweeps, suggesting that these selective forces have impacted genome-wide control of A. thaliana metabolism. Comparing the metabolic variation detected within this collection of wild accessions to a laboratory-derived population of recombinant inbred lines (derived from two of the accessions used in this study) showed that the higher level of genetic variation present within the wild accessions did not correspond to higher variance in metabolic phenotypes, suggesting that evolutionary constraints limit metabolic variation. While a major goal of genome-wide association studies is to develop catalogues of intraspecific variation, the results of multiple independent experiments performed for this study showed that the genotype-metabolite associations identified are sensitive to environmental fluctuations. Thus, studies of intraspecific variation conducted via genome-wide association will require analyses of genotype by environment interaction. Interestingly, the network structure of metabolite linkages was also sensitive to environmental differences, suggesting that key aspects of network architecture are malleable.     

Genetic variation in response to an indirect ecological effect

Indirect ecological effects (IEEs) are widespread and often as strong as the phenotypic effects arising from direct interactions in natural communities. Indirect effects can influence competitive interactions, and are thought to be important selective forces. However, the extent that selection arising from IEEs results in long-term evolutionary change depends on genetic variation underlying the phenotypic response-that is, a genotype-by-IEE interaction. We provide the first data on genetic variation in the response of traits to an IEE, and illustrate how such genetic variation might be detected and analysed. We used a model tri-trophic system to investigate the effect of host plants on two populations of predatory ladybirds through a clonal aphid herbivore. A split-family experimental design allowed us to estimate the effects of aphid host plant on ladybird traits (IEE) and the extent of genetic variation in ladybird predators for response to these effects (genotype-by-indirect environmental effect interaction). We found significant genetic variation in the response of ladybird phenotypes to the indirect effect of host plant of their aphid prey, demonstrating the potential for evolutionary responses to selection arising from the prey host.     

Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Genome-wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life-history trait

Understanding the genetic basis of traits involved in adaptation is a major challenge in evolutionary biology but remains poorly understood. Here, we use genome-wide association mapping using a custom 50 k single nucleotide polymorphism (SNP) array in a natural population of collared flycatchers to examine the genetic basis of clutch size, an important life-history trait in many animal species. We found evidence for an association on chromosome 18 where one SNP significant at the genome-wide level explained 3.9% of the phenotypic variance. We also detected two suggestive quantitative trait loci (QTLs) on chromosomes 9 and 26. Fitness differences among genotypes were generally weak and not significant, although there was some indication of a sex-by-genotype interaction for lifetime reproductive success at the suggestive QTL on chromosome 26. This implies that sexual antagonism may play a role in maintaining genetic variation at this QTL. Our findings provide candidate regions for a classic avian life-history trait that will be useful for future studies examining the molecular and cellular function of, as well as evolutionary mechanisms operating at, these loci.     

GENETIC VARIANCE AND COVARIANCE FOR PHYSIOLOGICAL TRAITS IN LOBELIA:ARE THERE CONSTRAINTS ON ADAPTIVE EVOLUTION?

Physiological traits that control the uptake of carbon dioxide and loss of water are key determinants of plant growth and reproduction. Variation in these traits is often correlated with environmental gradients of water, light, and nutrients, suggesting that natural selection is the primary evolutionary mechanism responsible for physiological diversification. Responses to selection, however, can be constrained by the amount of standing genetic variation for physiological traits and genetic correlations between these traits. To examine the potential for constraint on adaptive evolution, we estimated the quantitative genetic basis of physiological trait variation in one population of each of two closely related species (Lobelia siphilitica and L. cardinalis). Restricted maximum likelihood analyses of greenhouse-grown half-sib families were used to estimate genetic variances and covariances for seven traits associated with carbon and water relations. We detected significant genetic variation for all traits in L. siphilitica, suggesting that carbon-gain and water-use traits could evolve in response to natural selection in this population. In particular, narrow-sense heritabilities for photosynthetic rate (A), stomatal conductance (gs), and water-use efficiency (WUE) in our L. siphilitica population were high relative to previous studies in other species. Although there was significant narrow-sense heritability for A in L. cardinalis, we detected little genetic variation for traits associated with water use (gs and WUE), suggesting that our population of this species may be unable to adapt to drier environments. Despite being tightly linked functionally, the genetic correlation between A and gs was not strong and significant in either population. Therefore, our L. siphilitica population would not be genetically constrained from evolving high A (and thus fixing more carbon for growth and reproduction) while also decreasing gs to limit water loss. However, a significant negative genetic correlation existed between WUE and plant size in L. siphilitica, suggesting that high WUE may be negatively associated with high fecundity. In contrast, our results suggest that any constraints on the evolution of photosynthetic and stomatal traits of L. cardinalis are caused primarily by a lack of genetic variation, rather than by genetic correlations between these functionally related traits.     

Genetic variability under mutation selection balance

A fundamental problem in evolutionary genetics is understanding how high levels of genetic variation in quantitative traits are maintained in natural populations. Variation is removed by the natural selection of individuals with optimal phenotypes and is recovered by mutation; however, previous analyses had indicated that a mutation-selection balance was insufficient to maintain observed levels of genetic variation in these traits. Using more general models, however, it has recently been shown that it is indeed a sufficient mechanism. These models can be used to explore other phenomena in evolutionary biology.