Linking quantitative genetics with community-level performance: Are there operational models for plant breeding?

Plant breeding is focused on the genotype and population levels while targeting effects at higher levels of biodiversity, from crop covers to agroecosystems. Making predictions across nested levels of biodiversity is therefore a major challenge for the development of intercropping practices. New prediction tools and concepts are required to design breeding strategies with desirable outcomes at the crop community level. We reviewed theoretical advances in the field of evolutionary ecology to identify potentially operational ways of predicting the effects of artificial selection on community-level performances. We identified three main types of approaches differing in the way they model interspecific indirect genetic effects (IIGEs) at the community level: (1) The community heritability approach estimates the variance for IIGE induced by a focal species at the community level; (2) the joint phenotype approach quantifies genetic constraints between direct genetic effects and IIGE for a set of interacting species; (3) the community-trait genetic gradient approach decomposes the IIGE for a focal species across a multivariate set of its functional traits. We discuss the potential operational capacities of these approaches and stress that each is a special case of a general multitrait and multispecies selection index. Choosing one therefore involves assumptions and goals regarding the breeding target and strategy. Obtaining reliable quantitative, community-level predictions at the genetic level is constrained by the size and complexity of the experimental designs usually required. Breeding strategies should instead be compared using theoretically informed qualitative predictions. The need to estimate genetic covariances between traits measured both within and among species (for IIGE) is another obstacle, as the two are not determined by the exact same biological processes. We suggest future research directions and strategies to overcome these limits. Our synthesis offers an integrative theoretical framework for breeders interested in the genetic improvement of crop communities but also for scientists interested in the genetic bases of plant community functioning.

High-Throughput Genome-Wide Genotyping To Optimize the Use of Natural Genetic Resources in the Grassland Species Perennial Ryegrass (Lolium perenne L.).

The natural genetic diversity of agricultural species is an essential genetic resource for breeding programs aiming to improve their ecosystem and production services. A large natural ecotype diversity is usually available for most grassland species. This could be used to recombine natural climatic adaptations and agronomic value to create improved populations of grassland species adapted to future regional climates. However describing natural genetic resources can be long and costly. Molecular markers may provide useful information to help this task. This opportunity was investigated for Lolium perenne L., using a set of 385 accessions from the natural diversity of this species collected right across Europe and provided by genebanks of several countries. For each of these populations, genotyping provided the allele frequencies of 189,781 SNP markers. GWAS were implemented for over 30 agronomic and/or putatively adaptive traits recorded in three climatically contrasted locations (France, Belgium, Germany). Significant associations were detected for hundreds of markers despite a strong confounding effect of the genetic background; most of them pertained to phenology traits. It is likely that genetic variability in these traits has had an important contribution to environmental adaptation and ecotype differentiation. Genomic prediction models calibrated using natural diversity were found to be highly effective to describe natural populations for almost all traits as well as commercial synthetic populations for some important traits such as disease resistance, spring growth or phenological traits. These results will certainly be valuable information to help the use of natural genetic resources of other species.

Both selection and plasticity drive niche differentiation in experimental grasslands.

The way species avoid each other in a community by using resources differently across space and time is one of the main drivers of species coexistence in nature1,2. This mechanism, known as niche differentiation, has been widely examined theoretically but still lacks thorough experimental validation in plants. To shape niche differences over time, species within communities can reduce the overlap between their niches or find unexploited environmental space3. Selection and phenotypic plasticity have been advanced as two candidate processes driving niche differentiation4,5, but their respective role remains to be quantified6. Here, we tracked changes in plant height, as a candidate trait for light capture7, in 5-year multispecies sown grasslands. We found increasing among-species height differences over time. Phenotypic plasticity promotes this change, which explains the rapid setting of differentiation in our system. Through the inspection of changes in genetic structure, we also highlighted the contribution of selection. Altogether, we experimentally demonstrated the occurrence of species niche differentiation within artificial grassland communities over a short time scale through the joined action of both plasticity and selection.

Which Recurrent Selection Scheme To Improve Mixtures of Crop Species? Theoretical Expectations.

In a context of increasing environmental challenges, there is an emerging demand for plant cultivars that are adapted to cultivation in species mixture. It is thus pressing to look for the optimization of selection schemes to grow species mixtures, and especially recurrent selection schemes which are at the core of the improvement of many plant species. We considered the case of two populations from different species to be improved by recurrent selection for their performances in mixture. We set up an analytical model of performances in mixture. We expressed the expected responses of the performances in mixture to one cycle of selection in the case of a Reciprocal Mixture Ability selection scheme and of two parallel selection schemes aiming to improve General Mixture Abilities or performances in pure stands. We numerically compared these selection schemes when half-sib or topcross progeny families of selection candidates are tested in mixture. Selection in pure stands appeared efficient within a limited range of genetic correlations between pure stand performance and mixture model effects. The Reciprocal Mixture Ability selection scheme was expected to be less efficient than parallel selections for General Mixture Ability in some situations. The last option enables to control the ratio of expected responses of species contributions to the mixture performance without bias when using selection indices. When more than two species are be improved for their performances in mixture, the advantage of parallel selections for General Mixture Ability is even more marked, providing that compensation trends between species are not too prevalent.

Increasing the benefits of species diversity in multispecies temporary grasslands by increasing within-species diversity.

BACKGROUND AND AIMS: The positive effects of species diversity on the functioning and production of ecosystems have been discussed widely in the literature. In agriculture, these effects are increasingly being applied to mixed-species crops and particularly to temporary grasslands. However, the effects of increases in genetic diversity (i.e. within-species diversity) on productivity in multispecies crops have not been much studied. Nevertheless, genetic diversity may have strong positive effects on agricultural ecosystems and positively influence production and species abundances in multispecies covers. We examine here the effects of genetic diversity on temporary multispecies grasslands. METHODS: From a real situation, a breeder's field trial, we describe a study with five seed mixtures, each containing seven species (three grasses and four legumes) but with three different levels of genetic diversity (low, medium and high) created by using different numbers of cultivars per species. From the perspective of a plant breeder, we analyse measurements of biomass production over a 5-year period. KEY RESULTS: We show a positive effect of genetic diversity on production, on production stability and on the equilibrium of species abundances in the mixtures over the 5-year period of the experiment. The legume/grass proportions were best balanced, having the highest within-species diversity. CONCLUSIONS: For the first time in a field-plot study, we demonstrate the major role played by within-species genetic diversity on the production, stability and species composition of temporary grasslands. Our key results seem to find their explanation in terms of shifts in the peaks of species biomass production during the season, these shifts likely leading to temporal species complementarity. Our study suggests major benefits will arise with increases in the genetic diversity of multispecies crops. Genetic diversity may be useful in helping to meet new crop-diversification challenges, particularly with multispecies grasslands. Genetic and species diversity will likely provide additional levers for improving crops in diversified systems.

A generic individual-based model can predict yield, nitrogen content, and species abundance in experimental grassland communities.

Functional-structural plant models are increasingly being used to analyse relationships between plant functioning and the topological and spatial organisation of their modular structure. In this study, the performance of an individual-based model accounting for the the architecture and population dynamics of forage legumes in multi-species grasslands was assessed. Morphogenetic shoot and root parameters were calibrated for seven widely used species. Other model parameters concerning C and N metabolism were obtained from the literature. The model was evaluated using a series of independent experiments combining the seven species in binary mixtures that were subject to regular defoliation. For all the species, the model could accurately simulate phytomer demography, leaf area dynamics, and root growth under conditions of weak competition. In addition, the plastic changes induced by competition for light and N in terms of plant development, leaf area, N uptake, and total plant biomass were correctly predicted. The different species displayed contrasting sensitivities to defoliation, and the model was able to predict the superior ability of creeping species to sustain regular defoliation. As a result of competition and management, the balance between species changed over time and was strongly dependent on the pair of species used. The model proved able to capture these differences in community dynamics. Overall, the results demonstrate that integrating the individual components of population dynamics in a process-based model can provide good predictive capacity regarding mixtures of cultivated species.

A Conserved Potential Development Framework Applies to Shoots of Legume Species with Contrasting Morphogenetic Strategies.

A great variety of legume species are used for forage production and grown in multi-species grasslands. Despite their close phylogenetic relationship, they display a broad range of morphologies that markedly affect their competitive abilities and persistence in mixtures. Little is yet known about the component traits that control the deployment of plant architecture in most of these species. During the present study, we compared the patterns of shoot organogenesis and shoot organ growth in contrasting forage species belonging to the four morphogenetic groups previously identified in herbaceous legumes (i.e., stolon-formers, rhizome-formers, crown-formers tolerant to defoliation and crown-formers intolerant to defoliation). To achieve this, three greenhouse experiments were carried out using plant species from each group (namely alfalfa, birdsfoot trefoil, sainfoin, kura clover, red clover, and white clover) which were grown at low density under non-limiting water and soil nutrient availability. The potential morphogenesis of shoots characterized under these conditions showed that all the species shared a number of common morphogenetic features. All complied with a generalized classification of shoot axes into three types (main axis, primary and secondary axes). A common quantitative framework for vegetative growth and development involved: (i) the regular development of all shoot axes in thermal time and a deterministic branching pattern in the absence of stress; (ii) a temporal coordination of organ growth at the phytomer level that was highly conserved irrespective of phytomer position, and (iii) an identical allometry determining the surface area of all the leaves. The species differed in their architecture as a consequence of the values taken by component traits of morphogenesis. Assessing the relationships between the traits studied showed that these species were distinct from each other along two main PCA axes which explained 68% of total variance: the first axis captured a trade-off between maximum leaf size and the ability to produce numerous phytomers, while the second distinguished morphogenetic strategies reliant on either petiole or internode expansion to achieve space colonization. The consequences of this quantitative framework are discussed, along with its possible applications regarding plant phenotyping and modeling.

Five species, many genotypes, broad phenotypic diversity: When agronomy meets functional ecology.

PREMISE OF THE STUDY: Current ecological theory can provide insight into the causes and impacts of plant domestication. However, just how domestication has impacted intraspecific genetic variability (ITV) is unknown. We used 50 ecotypes and 35 cultivars from five grassland species to explore how selection drives functional trait coordination and genetic differentiation. METHODS: We quantified the extent of genetic diversity among different sets of functional traits and determined how much genetic diversity has been generated within populations of natural ecotypes and selected cultivars. KEY RESULTS: In general, the cultivars were larger (e.g., greater height, faster growth rates) and had larger and thinner leaves (greater SLA). We found large (average 63%) and trait-dependent (ranging from 14% for LNC to 95.8% for growth rate) genetic variability. The relative extent of genetic variability was greater for whole-plant than for organ-level traits. This pattern was consistent within ecotypes and within cultivars. However, ecotypes presented greater ITV variability. CONCLUSIONS: The results indicated that genetic diversity is large in domesticated species with contrasting levels of heritability among functional traits and that selection for high yield has led to indirect selection of some associated leaf traits. These findings open the way to define which target traits should be the focus in selection programs, especially in the context of community-level selection.

Diversity in Plant Breeding: A New Conceptual Framework.

Faced with an accelerating rate of environmental change and the associated need for a more sustainable, low-input agriculture, the urgent new challenge for crop science is to find ways to introduce greater diversity to cropping systems. However, there is a dearth of generic formalism in programs seeking to diversify crops. In this opinion, we propose a new framework, derived from ecological theory, that should enable diversity targets to be incorporated into plant-breeding programs. While ecological theory provides criteria for maintaining diversity and optimizing the production of mixtures, such criteria are rarely fully realized in natural ecosystems. Conversely, crop breeding should optimize both agronomic value and the ability of plants to perform and live alongside one another. This framework represents an opportunity to develop more sustainable crops and also a radical new way to apply ecological theory to cropping systems.

Spatial heterogeneity in landscape structure influences dispersal and genetic structure: empirical evidence from a grasshopper in an agricultural landscape.

Dispersal may be strongly influenced by landscape and habitat characteristics that could either enhance or restrict movements of organisms. Therefore, spatial heterogeneity in landscape structure could influence gene flow and the spatial structure of populations. In the past decades, agricultural intensification has led to the reduction in grassland surfaces, their fragmentation and intensification. As these changes are not homogeneously distributed in landscapes, they have resulted in spatial heterogeneity with generally less intensified hedged farmland areas remaining alongside streams and rivers. In this study, we assessed spatial pattern of abundance and population genetic structure of a flightless grasshopper species, Pezotettix giornae, based on the surveys of 363 grasslands in a 430-km² agricultural landscape of western France. Data were analysed using geostatistics and landscape genetics based on microsatellites markers and computer simulations. Results suggested that small-scale intense dispersal allows this species to survive in intensive agricultural landscapes. A complex spatial genetic structure related to landscape and habitat characteristics was also detected. Two P. giornae genetic clusters bisected by a linear hedged farmland were inferred from clustering analyses. This linear hedged farmland was characterized by high hedgerow and grassland density as well as higher grassland temporal stability that were suspected to slow down dispersal. Computer simulations demonstrated that a linear-shaped landscape feature limiting dispersal could be detected as a barrier to gene flow and generate the observed genetic pattern. This study illustrates the relevance of using computer simulations to test hypotheses in landscape genetics studies.

Complementary effects of species and genetic diversity on productivity and stability of sown grasslands.

Plant species diversity regulates the productivity(1-3) and stability(2,4) of natural ecosystems, along with their resilience to disturbance(5,6). The influence of species diversity on the productivity of agronomic systems is less clear(7-10). Plant genetic diversity is also suspected to influence ecosystem function(3,11-14), although empirical evidence is scarce. Given the large range of genotypes that can be generated per species through artificial selection, genetic diversity is a potentially important leverage of productivity in cultivated systems. Here we assess the effect of species and genetic diversity on the production and sustainable supply of livestock fodder in sown grasslands, comprising single and multispecies assemblages characterized by different levels of genetic diversity, exposed to drought and non-drought conditions. Multispecies assemblages proved more productive than monocultures when subject to drought, regardless of the number of genotypes per species present. Conversely, the temporal stability of production increased only with the number of genotypes present under both drought and non-drought conditions, and was unaffected by the number of species. We conclude that taxonomic and genetic diversity can play complementary roles when it comes to optimizing livestock fodder production in managed grasslands, and suggest that both levels of diversity should be considered in plant breeding programmes designed to boost the productivity and resilience of managed grasslands in the face of increasing environmental hazards.

Sex and space destabilize intransitive competition within and between species.

Organisms ranging from bacteria and corals to plants and vertebrates can form intransitive competitive networks, in which coexistence can be maintained because no one species or genotype is superior to all others. However, in the simplest case with three competing types, the long-term outcome may not be so clear if two of the three represent the ends of a continuous heritable trait distribution within one species, as has been recently demonstrated empirically in a short-term experiment with plants. Using simulation models of this scenario, results with asexual reproduction confirm previous studies which showed that local interactions promote coexistence. However, with sexual reproduction, genetic variance is reduced because selection fluctuates between favouring the two extremes during population cycles, while sex continually produces intermediates. Sex thus slows the response to selection when it is the strongest and therefore slows the recovery from extreme abundances, creating larger abundance fluctuations. Local interactions do not stabilize dynamics with sex because the resultant spatial patches of one species are genetically heterogeneous, such that particular phenotypes do not benefit from spatial refuges. In sharp contrast to previous models suggesting that sex or local interactions stabilize population dynamics, here sex and local interactions destabilize dynamics and increase extinction risk.

Genetic structure and gene flow along an altitudinal gradient among two stomoxyine species (Diptera: Muscidae) on La Réunion Island.

Seasonal variations of insect population sizes are often dramatic, particularly in temperate regions and at altitudes where the climatic conditions are unfavorable to insect development during the winter. Decline of population size (or bottlenecks) and founder events may reduce the genetic variability and may create genetic differentiation between populations by drift and founder effects, but this reduction of genetic diversity is strongly influenced by gene flow between populations. In this study, we determined the population genetic structure for two stomoxyine species (Diptera: Muscidae), Stomoxys calcitrans (L.) and Stomoxys niger niger Macquart, which co-occur in dairy barns along an altitudinal gradient on La Réunion island. Using microsatellite markers, we quantified the genetic variation within and among populations for different altitudes. This study displays that, contrary to expectations, genetic diversity is not correlated with altitude and that genetic differentiation is not larger among high-altitude populations than among low-altitude populations. These results attest to the small drift and founder effects in high-altitude populations despite drastic decreases in population size during the winter. Furthermore, at the island scale, the populations of S. calcitrans were slightly differentiated, but those of S. niger niger were not. Together, the results revealed large levels of gene flow on La Réunion Island despite the dramatic geographic barriers, and they emphasize the importance of considering agricultural practices to restrict the dispersal of stomoxyines.