The emotion system promotes diversity and evolvability

Studies on the relationship between the optimal phenotype and its environment have had limited focus on genotype-to-phenotype pathways and their evolutionary consequences. Here, we study how multi-layered trait architecture and its associated constraints prescribe diversity. Using an idealized model of the emotion system in fish, we find that trait architecture yields genetic and phenotypic diversity even in absence of frequency-dependent selection or environmental variation. That is, for a given environment, phenotype frequency distributions are predictable while gene pools are not. The conservation of phenotypic traits among these genetically different populations is due to the multi-layered trait architecture, in which one adaptation at a higher architectural level can be achieved by several different adaptations at a lower level. Our results emphasize the role of convergent evolution and the organismal level of selection. While trait architecture makes individuals more constrained than what has been assumed in optimization theory, the resulting populations are genetically more diverse and adaptable. The emotion system in animals may thus have evolved by natural selection because it simultaneously enhances three important functions, the behavioural robustness of individuals, the evolvability of gene pools and the rate of evolutionary innovation at several architectural levels.     

Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family

Arabidopsis thaliana provides a scientifically attractive and simple model for studying root growth and architecture and, subsequently, for discovering new genes involved in the control of these characters in plants. We have used the natural variation available in Arabidopsis accessions and mapped quantitative trait loci (QTLs) for primary root length (PRL), lateral root number (LRN) and density (LRD) and for total length of the lateral root system (LRL) in the Bay-0 × Shahdara population. Total phenotypic variation was very large, and despite the importance of the environmental component we were able to map 13 QTLs and one epistatic interaction between QTLs. Our results highlight the biological relevance and genetic control of lateral root density in this material. We were also able to show that variation in the extent of the lateral root system depends mainly on the growth of the existing lateral roots rather than in a change in LRN. Factors controlling lateral root growth seemed to have no major effect on primary root growth. Moreover, Shahdara QTL alleles always increased the length of the lateral roots, which may be taken as an adaptation to its very dry natural environment in Tadjikistan. A QTL for PRL was confirmed using a type of near-isogenic line called a heterogeneous inbred family (HIF), and this QTL is a candidate for further fine-mapping and cloning.     

Application of Brachypodium to the genetic improvement of wheat roots

To meet the demands of a larger and more affluent global population, wheat yields must increase faster this century than last, with less irrigation, fertilizer, and land. Modelling and experiments consistently demonstrate a large potential for increasing wheat productivity by improving root systems; however, application of research to new varieties is slow because of the inherent difficulties associated with working underground. This review makes the case for the use of the model grass Brachypodium distachyon to simplify root research and accelerate the identification of genes underlying wheat root improvement. Brachypodium is a small temperate grass with many genomic, genetic, and experimental resources that make it a tractable model plant. Brachypodium and wheat have very similar root anatomies which are distinct from rice root anatomy that is specialized to help it overcome anaerobic conditions associated with submerged roots. As a dicotyledonous plant, Arabidopsis has an even more divergent root system that features a tap root system and cambia with secondary growth, both of which are lacking in the grasses. The major advantage of Brachypodium is its small stature that allows the adult grass root system to be readily phenotyped, unlike rice and maize. This will facilitate the identification of genes in adult roots that greatly influence yield by modulating water uptake during flowering and grain development. A summary of the advantages of Brachypodium for root studies is presented, including the adult root system architecture and root growth during grain development. Routes to translate discoveries from Brachypodium to wheat are also discussed.     

Mapping quantitative trait loci in multiple populations of Arabidopsis thaliana identifies natural allelic variation for trichome density

The majority of biological traits are genetically complex. Mapping the quantitative trait loci (QTL) that determine these phenotypes is a powerful means for estimating many parameters of the genetic architecture for a trait and potentially identifying the genes responsible for natural variation. Typically, such experiments are conducted in a single mapping population and, therefore, have only the potential to reveal genomic regions that are polymorphic between the progenitors of the population. What remains unclear is how well the QTL identified in any one mapping experiment characterize the genetics that underlie natural variation in traits. Here we provide QTL mapping data for trichome density from four recombinant inbred mapping populations of Arabidopsis thaliana. By aligning the linkage maps for these four populations onto a common physical map, the results from each experiment were directly compared. Seven of the nine QTL identified are population specific while two were mapped in all four populations. Our results show that many lineage-specific alleles that either increase or decrease trichome density persist in natural populations and that most of this genetic variation is additive. More generally, these findings suggest that the use of multiple populations holds great promise for better understanding the genetic architecture of natural variation.     

Patterns of genetic diversity vary among shoot and root functional traits in Norway spruce Picea abies along a latitudinal gradient

Roots constitute a major segment of plant biomass, and variation in belowground traits in situ correlates with environmental gradients at large spatial scales. Local adaptation of populations maintains intraspecific genetic variation in various shoot traits, but the contribution of genetic factors to adaptation to soil heterogeneity remains poorly known. I established a common-garden experiment with three Norway spruce Picea abies populations sampled between 60° and 67° N in Finland, each represented by 13 or 15 maternal families, to determine whether belowground traits are as genetically differentiated among populations as those in the shoot along a collective latitudinal gradient of temperature and soil heterogeneity. Two growing season simulations enabled testing for among-population differences in phenotypic plasticity. I phenotyped 777 first-year seedlings from shoot to root to capture functional traits that may influence survival in the wild: autumn phenology, shoot growth, root system size, root architecture, root morphology and growth allocation. All traits exhibited within-population genetic diversity, but among-population differentiation ranged from strong in shoot traits to nonexistent in root system architecture and morphology that are scaled to root system size. However, latitudinal trends characterised root-to-shoot ratio and root tip-to-shoot ratio that account for among-population differences in aboveground growth. Overall trait variability was multidimensional with variable among- versus within-population trends: for example, phenology and shoot growth covaried across populations, but their association within individual populations was variable. Shoot growth correlated positively with root system size, but not with root architecture or morphology. Finally, the two higher-latitude populations exhibited greater phenotypic plasticity in shoot traits and growth allocation. The results demonstrate varying patterns of genetic variation in functional traits of Norway spruce in the boreal zone, suggesting simultaneous adaptation to multiple environmental factors. Functional traits that exhibit phenotypic plasticity, genetic diversity and little covariation will promote long-term survival of populations in fluctuating environments.     

Similarity in G matrix structure among natural populations of Arabidopsis lyrata

Understanding the stability of the G matrix in natural populations is fundamental for predicting evolutionary trajectories; yet, the extent of its spatial variation and how this impacts responses to selection remain open questions. With a nested paternal half‐sib crossing design and plants grown in a field experiment, we examined differences in the genetic architecture of flowering time, floral display, and plant size among four Scandinavian populations of Arabidopsis lyrata. Using a multivariate Bayesian framework, we compared the size, shape, and orientation of G matrices and assessed their potential to facilitate or constrain trait evolution. Flowering time, floral display and rosette size varied among populations and significant additive genetic variation within populations indicated potential to evolve in response to selection. Yet, some characters, including flowering start and number of flowers, may not evolve independently because of genetic correlations. Using a multivariate framework, we found few differences in the genetic architecture of traits among populations. G matrices varied mostly in size rather than shape or orientation. Differences in multivariate responses to selection predicted from differences in G were small, suggesting overall matrix similarity and shared constraints to trait evolution among populations.     

Natural variation in Arabidopsis thaliana revealed a genetic network controlling germination under salt stress

Plant responses to environmental stresses are polygenic and complex traits. In this study quantitative genetics using natural variation in Arabidopsis thaliana was used to investigate the genetic architecture of plant responses to salt stress. Eighty seven A. thaliana accessions were screened and showed a large variation for root development and seed germination under 125 and 200 mM NaCl, respectively. Twenty two quantitative trait loci for these traits have been detected by phenotyping two recombinants inbred line populations, Sha x Col and Sha x Ler. Four QTLs controlling germination under salt were detected in the Sha x Col population. Interestingly, only one allelic combination at these four QTLs inhibits germination under salt stress, implying strong epistatic interactions between them. In this interacting context, we confirmed the effect of one QTL by phenotyping selected heterozygous inbred families. We also showed that this QTL is involved in the control of germination under other stress conditions such as KCl, mannitol, cold, glucose and ABA. Our data highlights the presence of a genetic network which consists of four interacting QTLs and controls germination under limiting environmental conditions.     

The genetic architecture of sexually selected traits in two natural populations of Drosophila montana

We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. To study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major quantitative trait loci (QTLs) were detected, perhaps because the between-population QTLs were due to fixed differences between the populations. Partitioning the trait variation to chromosomes suggested a broadly polygenic genetic architecture of within-population variation, although some chromosomes explained more variation in one population compared with the other. Studies of natural variation provide an important contrast to crosses between species or divergent lines, but our analysis highlights recent concerns that segregating variation within populations for important quantitative ecological traits may largely consist of small effect alleles, difficult to detect with studies of moderate power.     

Identification of quantitative trait loci that regulate Arabidopsis root system size and plasticity

Root system size (RSS) is a complex trait that is greatly influenced by environmental cues. Hence, both intrinsic developmental pathways and environmental-response pathways contribute to RSS. To assess the natural variation in both types of pathways, we examined the root systems of the closely related Arabidopsis ecotypes Landsberg erecta (Ler) and Columbia (Col) grown under mild osmotic stress conditions. We found that Ler initiates more lateral root primordia, produces lateral roots from a higher percentage of these primordia, and has an overall larger root system than Col under these conditions. Furthermore, although each of these parameters is reduced by osmotic stress in both ecotypes, Ler shows a decreased sensitivity to osmotica. To understand the genetic basis for these differences, QTL for RSS under mild osmotic stress were mapped in a Ler x Col recombinant inbred population. Two robust quantitative trait loci (QTL) were identified and confirmed in near-isogenic lines (NILs). The NILs also allowed us to define distinct physiological roles for the gene(s) at each locus. This study provides insight into the genetic and physiological complexity that determines RSS and begins to dissect the molecular basis for naturally occurring differences in morphology and developmental plasticity in the root system.     

Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216‐year time series of Arabidopsis thaliana accessions from across its native range and applied spatially varying coefficient models to quantify region‐specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space or through time. For example, δ¹⁵N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer‐ versus spring‐collected plants, consistent with a life history–physiology axis from slow‐growing winter annuals to fast‐growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.     

Investigating the genetic architecture of conditional strategies using the environmental threshold model

The threshold expression of dichotomous phenotypes that are environmentally cued or induced comprise the vast majority of phenotypic dimorphisms in colour, morphology, behaviour and life history. Modelled as conditional strategies under the framework of evolutionary game theory, the quantitative genetic basis of these traits is a challenge to estimate. The challenge exists firstly because the phenotypic expression of the trait is dichotomous and secondly because the apparent environmental cue is separate from the biological signal pathway that induces the switch between phenotypes. It is the cryptic variation underlying the translation of cue to phenotype that we address here. With a ‘half-sib common environment’ and a ‘family-level split environment’ experiment, we examine the environmental and genetic influences that underlie male dimorphism in the earwig Forficula auricularia. From the conceptual framework of the latent environmental threshold (LET) model, we use pedigree information to dissect the genetic architecture of the threshold expression of forceps length. We investigate for the first time the strength of the correlation between observable and cryptic ‘proximate’ cues. Furthermore, in support of the environmental threshold model, we found no evidence for a genetic correlation between cue and the threshold between phenotypes. Our results show strong correlations between observable and proximate cues and less genetic variation for thresholds than previous studies have suggested. We discuss the importance of generating better estimates of the genetic variation for thresholds when investigating the genetic architecture and heritability of threshold traits. By investigating genetic architecture by means of the LET model, our study supports several key evolutionary ideas related to conditional strategies and improves our understanding of environmentally cued decisions.     

Natural variation of hormone levels in Arabidopsis roots and correlations with complex root architecture

Studies on natural variation are an important tool to unravel the genetic basis of quantitative traits in plants.Despite the significant roles of phytohormones in plant development, including root architecture, hardly any studies have been done to investigate natural variation in endogenous hormone levels in plants. Therefore, in the present study a range of hormones were quantified in root extracts of thirteen Arabidopsis thaliana accessions using a ultra performance liquid chromatography triple quadrupole mass spectrometer.Root system architecture of the set of accessions was quantified, using a new parameter(mature root unit) for complex root systems, and correlated with the phytohormone data. Significant variations in phytohormone levels among the accessions were detected, but were remarkably small, namely less than three-fold difference between extremes. For cytokinins, relatively larger variations were found for ribosides and glucosides, as compared to the free bases. For root phenotyping, length-related traits—lateral root length and total root length—showed larger variations than lateral root number-related ones. For root architecture, antagonistic interactions between hormones, for example, indole-3-acetic acid to trans-zeatin were detected in correlation analysis.These findings provide conclusive evidence for the presence of natural variation in phytohormone levels in Arabidopsis roots,suggesting that quantitative genetic analyses are feasible.     

Genome-Wide Association Analysis of Adaptation Using Environmentally Predicted Traits

Current methods for studying the genetic basis of adaptation evaluate genetic associations with ecologically relevant traits or single environmental variables, under the implicit assumption that natural selection imposes correlations between phenotypes, environments and genotypes. In practice, observed trait and environmental data are manifestations of unknown selective forces and are only indirectly associated with adaptive genetic variation. In theory, improved estimation of these forces could enable more powerful detection of loci under selection. Here we present an approach in which we approximate adaptive variation by modeling phenotypes as a function of the environment and using the predicted trait in multivariate and univariate genome-wide association analysis (GWAS). Based on computer simulations and published flowering time data from the model plant Arabidopsis thaliana, we find that environmentally predicted traits lead to higher recovery of functional loci in multivariate GWAS and are more strongly correlated to allele frequencies at adaptive loci than individual environmental variables. Our results provide an example of the use of environmental data to obtain independent and meaningful information on adaptive genetic variation.     

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.     

Natural variation of the root morphological response to nitrate supply in Arabidopsis thaliana

Nitrogen fertilization increases crop yield but excessive nitrate use can be a major environmental problem due to soil leaching or greenhouse gas emission. Root traits have been seldom considered as selection criteria to improve Nitrogen Use Efficiency of crops, due to the difficulty of measuring root traits under field conditions. Nonetheless, learning about mechanisms of lateral root (LR) growth stimulation or repression by nitrate availability could help to redesign root system architecture (RSA), a strategy aimed at developing plants with a dense and profound root system and with higher N uptake efficiency. Here, we explored the genetic diversity provided by natural populations of the model species Arabidopsis thaliana to identify potentially adaptive differences in biomass production and root morphology in response to nitrate availability. A core collection of 24 accessions that maximizes the genetic diversity within the species and Col-0 (the reference accession) were grown vertically on agar medium at moderate (N+) nitrate level for 6 days and then transferred to the same condition or to low (N?) nitrate concentration for 7 days. There was a major nutritional effect on the shoot biomass and root to shoot biomass ratio. The variation of the root biomass and RSA traits (primary root length, LRs number, LR mean length, total LRs length and LR densities) was primarily genetically determined. Differences in RSA traits between accessions were somewhat more pronounced at N?. Some accessions produced almost no visible LRs (Pyl-1, N13) at N?, while other produced up to a dozen (Kn-0). Taken together our data illustrate that natural variation exists within Arabidopsis for the studied traits. The identification of RSA ideotypes in the N response will facilitate further analysis of quantitative traits for root morphology.     

How to be early flowering: an evolutionary perspective

In wild and cultivated annual plant species, flowering time is an important life-history trait that coordinates the life cycle with local environmental conditions. Extensive studies on the genetic basis of flowering time in the model species Arabidopsis thaliana have revealed a complex genetic network that can detect environmental and internal signals. Based on this knowledge and on known pleiotropic effects associated with flowering time genes, we suggest that a natural shift towards an early-flowering life cycle might involve only particular functional regions in a limited number of genes. Our predictions are supported by genetic theories of adaptation and by recent data about genes associated with natural variation. We analyse the extent to which these predictions can also apply to crop species.     

Root system architecture: opportunities and constraints for genetic improvement of crops

Abiotic stresses increasingly curtail crop yield as a result of global climate change and scarcity of water and nutrients. One way to minimize the negative impact of these factors on yield is to manipulate root system architecture (RSA) towards a distribution of roots in the soil that optimizes water and nutrient uptake. It is now established that most of the genetic variation for RSA is driven by a suite of quantitative trait loci. As we discuss here, marker-assisted selection and quantitative trait loci cloning for RSA are underway, exploiting genomic resources, candidate genes and the knowledge gained from Arabidopsis, rice and other crops. Nonetheless, efficient and accurate phenotyping, modelling and collaboration with breeders remain important challenges, particularly when defining ideal RSA for different crops and target environments.     

Heritability of interpack aggression in a wild pedigreed population of North American grey wolves

Aggression is a quantitative trait deeply entwined with individual fitness. Mapping the genomic architecture underlying such traits is complicated by complex inheritance patterns, social structure, pedigree information and gene pleiotropy. Here, we leveraged the pedigree of a reintroduced population of grey wolves (Canis lupus) in Yellowstone National Park, Wyoming, USA, to examine the heritability of and the genetic variation associated with aggression. Since their reintroduction, many ecological and behavioural aspects have been documented, providing unmatched records of aggressive behaviour across multiple generations of a wild population of wolves. Using a linear mixed model, a robust genetic relationship matrix, 12,288 single nucleotide polymorphisms (SNPs) and 111 wolves, we estimated the SNP‐based heritability of aggression to be 37% and an additional 14% of the phenotypic variation explained by shared environmental exposures. We identified 598 SNP genotypes from 425 grey wolves to resolve a consensus pedigree that was included in a heritability analysis of 141 individuals with SNP genotype, metadata and aggression data. The pedigree‐based heritability estimate for aggression is 14%, and an additional 16% of the phenotypic variation was explained by shared environmental exposures. We find strong effects of breeding status and relative pack size on aggression. Through an integrative approach, these results provide a framework for understanding the genetic architecture of a complex trait that influences individual fitness, with linkages to reproduction, in a social carnivore. Along with a few other studies, we show here the incredible utility of a pedigreed natural population for dissecting a complex, fitness‐related behavioural trait.     

Exploiting the Brachypodium Tool Box in cereal and grass research

It is now a decade since Brachypodium distachyon (Brachypodium) was suggested as a model species for temperate grasses and cereals. Since then transformation protocols, large expressed sequence tag (EST) databases, tools for forward and reverse genetic screens, highly refined cytogenetic probes, germplasm collections and, recently, a complete genome sequence have been generated. In this review, we will describe the current status of the Brachypodium Tool Box and how it is beginning to be applied to study a range of biological traits. Further, as genomic analysis of larger cereals and forage grasses genomes are becoming easier, we will re-evaluate Brachypodium as a model species. We suggest that there remains an urgent need to employ reverse genetic and functional genomic approaches to identify the functionality of key genetic elements, which could be employed subsequently in plant breeding programmes; and a requirement for a Pooideae reference genome to aid assembling large pooid genomes. Brachypodium is an ideal system for functional genomic studies, because of its easy growth requirements, small physical stature, and rapid life cycle, coupled with the resources offered by the Brachypodium Tool Box.     

Strong population structure characterizes weediness gene evolution in the invasive grass species Brachypodium distachyon

Mediterranean annual grasses have invaded California and have replaced vast areas of native grassland. One of these invasive grasses is Brachypodium distachyon , a new model species for the grasses with extensive genomic resources and a nearly completed genome sequence. This study shows that the level of genetic variation in invaded California grasslands is lower compared to the native range in Eurasia. The invaded regions are characterized by highly differentiated populations of B. distachyon isolated by distance, most likely as a result of founder effects and a dearth of outcrossing events. EXP6 and EXP10 encoding α-expansins responsible for rapid growth, and AGL11 and AGL13 encoding proteins involved in vegetative phase regulation, appear to be under purifying selection with no evidence for local adaptation. Our data show that B. distachyon has diverged only recently from related Brachypodium species and that tetraploidization might have been as recent as a few thousand years ago. Observed low genetic variation in EXP10 and AGL13 appears to have been present in Eurasia before tetraploidization, potentially as a result of strong selective pressures on advantageous mutations, which are most likely responsible for its fast growth and rapid completion of its life cycle.