Advancing research on ectomycorrhizal fungal adaptation with landscape genomics

Ectomycorrhizal (ECM) fungi serve key functions in forest ecosystems by supplying water and nutrients to tree hosts, yet mutualistic plant–fungi interactions are jeopardised by environmental alterations. Here, we discuss the great potential and current limitations of landscape genomics in investigating signatures of local adaptation in natural populations of ECM fungi.     

Landscape genomics and a common garden trial reveal adaptive differentiation to temperature across Europe in the tree species Alnus glutinosa

The adaptive potential of tree species to cope with climate change has important ecological and economic implications. Many temperate tree species experience a wide range of environmental conditions, suggesting high adaptability to new environmental conditions. We investigated adaptation to regional climate in the drought‐sensitive tree species Alnus glutinosa (Black alder), using a complementary approach that integrates genomic, phenotypic and landscape data. A total of 24 European populations were studied in a common garden and through landscape genomic approaches. Genotyping‐by‐sequencing was used to identify SNPs across the genome, resulting in 1990 SNPs. Although a relatively low percentage of putative adaptive SNPs was detected (2.86% outlier SNPs), we observed clear associations among outlier allele frequencies, temperature and plant traits. In line with the typical drought avoiding nature of A. glutinosa, leaf size varied according to a temperature gradient and significant associations with multiple outlier loci were observed, corroborating the ecological relevance of the observed outlier SNPs. Moreover, the lack of isolation by distance, the very low genetic differentiation among populations and the high intrapopulation genetic variation all support the notion that high gene exchange combined with strong environmental selection promotes adaptation to environmental cues.     

Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding

Forest trees are an unparalleled group of organisms in their combined ecological, economic and societal importance. With widespread distributions, predominantly random mating systems and large population sizes, most tree species harbour extensive genetic variation both within and among populations. At the same time, demographic processes associated with Pleistocene climate oscillations and land‐use change have affected contemporary range‐wide diversity and may impinge on the potential for future adaptation. Understanding how these adaptive and neutral processes have shaped the genomes of trees species is therefore central to their management and conservation. As for many other taxa, the advent of high‐throughput sequencing methods is expected to yield an understanding of the interplay between the genome and environment at a level of detail and depth not possible only a few years ago. An international conference entitled ‘Genomics and Forest Tree Genetics’ was held in May 2016, in Arcachon (France), and brought together forest geneticists with a wide range of research interests to disseminate recent efforts that leverage contemporary genomic tools to probe the population, quantitative and evolutionary genomics of trees. An important goal of the conference was to discuss how such data can be applied to both genome‐enabled breeding and the conservation of forest genetic resources under land use and climate change. Here, we report discoveries presented at the meeting and discuss how the ecological genomic toolkit can be used to address both basic and applied questions in tree biology.     

Range margin populations show high climate adaptation lags in European trees

How populations of long‐living species respond to climate change depends on phenotypic plasticity and local adaptation processes. Marginal populations are expected to have lags in adaptation (i.e. differences between the climatic optimum that maximizes population fitness and the local climate) because they receive pre‐adapted alleles from core populations preventing them from reaching a local optimum in their climatically marginal habitat. Yet, whether adaptation lags in marginal populations are a common feature across phylogenetically and ecologically different species and how lags can change with climate change remain unexplored. To test for range‐wide patterns of phenotypic variation and adaptation lags of populations to climate, we (a) built model ensembles of tree height accounting for the climate of population origin and the climate of the site for 706 populations monitored in 97 common garden experiments covering the range of six European forest tree species; (b) estimated populations' adaptation lags as the differences between the climatic optimum that maximizes tree height and the climate of the origin of each population; (c) identified adaptation lag patterns for populations coming from the warm/dry and cold/wet margins and from the distribution core of each species range. We found that (a) phenotypic variation is driven by either temperature or precipitation; (b) adaptation lags are consistently higher in climatic margin populations (cold/warm, dry/wet) than in core populations; (c) predictions for future warmer climates suggest adaptation lags would decrease in cold margin populations, slightly increasing tree height, while adaptation lags would increase in core and warm margin populations, sharply decreasing tree height. Our results suggest that warm margin populations are the most vulnerable to climate change, but understanding how these populations can cope with future climates depend on whether other fitness‐related traits could show similar adaptation lag patterns.     

Tree diseases and landscape processes: the challenge of landscape pathology

Forest pathology inherently involves a landscape perspective, because tree pathogens propagate according to heterogeneous spatial patterns of flow and isolation. Landscape pathology is a field that is now emerging from the transdisciplinary cooperation of forest pathologists with landscape ecologists. Here, we review recent broad-scale assessments of tree disease risk, investigations of site and host preferences for several root rot pathogens, and regional historical analyses of pathogen outbreak in plantations. Crucial topics include fragmentation effects on pathogen spread and geophysical features that predispose forest patches to disease expression. Recent methodological developments facilitate the spatially explicit analysis of reciprocal coarse-scale relationships among hosts and pathogens. Landscape pathology studies fill a significant research gap in the context of our understanding of sustainable forest management, the introduction of exotic organisms and how climate change might affect the spread of disease.     

Opinion: Is gene mapping in wild populations useful for understanding and predicting adaptation to global change?

Changing environmental conditions will inevitably alter selection pressures. Over the long term, populations have to adapt to these altered conditions by evolutionary change to avoid extinction. Quantifying the ‘evolutionary potential’ of populations to predict whether they will be able to adapt fast enough to forecasted changes is crucial to fully assess the threat for biodiversity posed by climate change. Technological advances in sequencing and high‐throughput genotyping have now made genomic studies possible in a wide range of species. Such studies, in theory, allow an unprecedented understanding of the genomics of ecologically relevant traits and thereby a detailed assessment of the population's evolutionary potential. Aimed at a wider audience than only evolutionary geneticists, this paper gives an overview of how gene‐mapping studies have contributed to our understanding and prediction of evolutionary adaptations to climate change, identifies potential reasons why their contribution to understanding adaptation to climate change may remain limited, and highlights approaches to study and predict climate change adaptation that may be more promising, at least in the medium term.     

An essay on the necessity and feasibility of conservation genomics

The basic premise of conservation genetics is that small populations may be genetically threatened. The two steps leading to this premise are: (1) due to prominent influence of random genetic drift and inbreeding allelic and genotypic diversity in small populations is expected to be low, and (2) low allelic diversity and high homozygosity are expected to lead to immediate fitness decreases (inbreeding depression) and a compromised potential for evolutionary adaptation. Conservation genetic research has been strongly stimulated by the application of neutral molecular markers like microsatellites and AFLPs. In general these marker studies have provided evidence for step 1. It is less evident how these markers may provide evidence for step 2. In this essay we argue that, in order to get detailed insight in step 2, adopting a conservation genomic approach, in which conservation genetics will use approaches from ecological and evolutionary functional genomics (ecogenomics), is both necessary and feasible. Conservation genomics is necessary for studying functional genomic variation as function of drift and inbreeding, for studying the mechanisms that relate low genetic variation to low fitness, for integrating environmental and genetic approaches to conservation biology, and for developing modern, fast monitoring tools. The rapid technical and financial developments in genomics currently make conservation genomics feasible, and will improve feasibility in the very near future even further. We therefore argue that conservation genomics personifies part of the near future of conservation genetics.     

Ecological genomics meets community‐level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation

Local adaptation is a central feature of most species occupying spatially heterogeneous environments, and may factor critically in responses to environmental change. However, most efforts to model the response of species to climate change ignore intraspecific variation due to local adaptation. Here, we present a new perspective on spatial modelling of organism–environment relationships that combines genomic data and community‐level modelling to develop scenarios regarding the geographic distribution of genomic variation in response to environmental change. Rather than modelling species within communities, we use these techniques to model large numbers of loci across genomes. Using balsam poplar (Populus balsamifera) as a case study, we demonstrate how our framework can accommodate nonlinear responses of loci to environmental gradients. We identify a threshold response to temperature in the circadian clock gene GIGANTEA‐5 (GI5), suggesting that this gene has experienced strong local adaptation to temperature. We also demonstrate how these methods can map ecological adaptation from genomic data, including the identification of predicted differences in the genetic composition of populations under current and future climates. Community‐level modelling of genomic variation represents an important advance in landscape genomics and spatial modelling of biodiversity that moves beyond species‐level assessments of climate change vulnerability.     

Optimizing sampling design and sequencing strategy for the genomic analysis of quantitative traits in natural populations

Mapping the genes underlying ecologically relevant traits in natural populations is fundamental to develop a molecular understanding of species adaptation. Current sequencing technologies enable the characterization of a species’ genetic diversity across the landscape or even over its whole range. The relevant capture of the genetic diversity across the landscape is critical for a successful genetic mapping of traits and there are no clear guidelines on how to achieve an optimal sampling and which sequencing strategy to implement. Here we determine, through simulation, the sampling scheme that maximizes the power to map the genetic basis of a complex trait in an outbreeding species across an idealized landscape and draw genomic predictions for the trait, comparing individual and pool sequencing strategies. Our results show that quantitative trait locus detection power and prediction accuracy are higher when more populations over the landscape are sampled and this is more cost-effectively done with pool sequencing than with individual sequencing. Additionally, we recommend sampling populations from areas of high genetic diversity. As progress in sequencing enables the integration of trait-based functional ecology into landscape genomics studies, these findings will guide study designs allowing direct measures of genetic effects in natural populations across the environment.     

From population genetics to population genomics of forest trees: integrated population genomics approach

Early works by Altukhov and his associates on pine and spruce laid the foundation for Russian population genetic studies on tree species with the use of molecular genetic markers. In recent years, these species have become especially popular as nontraditional eukaryotic models for population and evolutionary genomic research. Tree species with large, cross-pollinating native populations, high genetic and phenotypic variation, growing in diverse environments and affected by environmental changes during hundreds of years of their individual development, are an ideal model for studying the molecular genetic basis of adaptation. The great advance in this field is due to the rapid development of population genomics in the last few years. In the broad sense, population genomics is a novel, fast-developing discipline, combining traditional population genetic approaches with the genomic level of analysis. Thousands of genes with known function and sometimes known genomic localization can be simultaneously studied in many individuals. This opens new prospects for obtaining statistical estimates for a great number of genes and segregating elements. Mating system, gene exchange, reproductive population size, population disequilibrium, interaction among populations, and many other traditional problems of population genetics can be now studied using data on variation in many genes. Moreover, population genomic analysis allows one to distinguish factors that affect individual genes, alleles, or nucleotides (such as, for example, natural selection) from factors affecting the entire genome (e.g., demography). This paper presents a brief review of traditional methods of studying genetic variation in forest tree species and introduces a new, integrated population genomics approach. The main stages of the latter are : (1) selection of genes, which are tentatively involved in variation of adaptive traits, by means of a detailed examination of the regulation and the expression of individual genes and genotypes, with subsequent determination of their complete allelic composition by direct nucleotide sequencing; (2) examination of the phenotypic effects of individual alleles by, e.g., association mapping; and (3) determining the frequencies of the selected alleles in natural population for identification of the adaptive variation pattern in the heterogeneous environment. Through decoding the phenotypic effects of individual alleles and identification of adaptive variation patterns at the population level, population genomics in the future will serve as a very helpful, efficient, and economical tool, essential for developing a correct strategy for conserving and increasing forests and other commercially valuable plant and animal species.     

Stand Structural Dynamics of North American Boreal Forests

Stand structure, the arrangement and interrelationships of live and dead trees, has been linked to forest regeneration, nutrient cycling, wildlife habitat, and climate regulation. The objective of this review was to synthesize literature on stand structural dynamics of North American boreal forests, addressing both live tree and coarse woody debris (CWD) characteristics under different disturbance mechanisms (fire, clearcut, wind, and spruce budworm), while identifying regional differences based on climate and surficial deposit variability. In fire origin stands, both live tree and CWD attributes are influenced initially largely by the characteristics of the stand replacing fire and later increasingly by autogenic processes. Differences in stand structure have also been observed between various stand cover types. Blowdown and insect outbreaks are two significant non-stand replacing disturbances that can alter forest stand structure through removing canopy trees, freeing up available growing space, and creating microsites for new trees to establish. Climate and surficial deposits are highly variable in the boreal forest due to its extensive geographic range, influencing stand and landscape structure by affecting tree colonization, stand composition, successional trajectories, CWD dynamics, and disturbance regimes including regional fire cycles. Further, predicted climate change scenarios are likely to cause regional-specific alterations in stand and landscape structure, with the implications on ecosystem components including wildlife, biodiversity, and carbon balance still unclear. Some stand structural attributes are found to be similar between clearcut and fire origin stands, but others appear to be quite different. Future research shall focus on examining structural variability under both disturbance regimes and management alternatives emulating both stand replacing and non-stand replacing natural disturbances.

     

Climate and fragmentation affect forest structure at the southern border of Amazonia

Background: The remaining forests in the extensive contact zone between southern Amazonia (seasonal rain forest) and the Cerrado (savanna) biomes are at risk due to intense land-use and climate change.

Aims: To explore the vulnerability of these transitional forests to changes in land use and climate, we evaluated the effects of fragmentation and climatic variables on forest structure.

Methods: We measured the diameter and height of 14,185 trees with diameter ≥10 cm at 24 forest plots distributed over an area of 25,000 km². For each plot, we obtained data on contemporary fragmentation and climatic variables.

Results: Forest structure variables (height, diameter, height:diameter allometry, biomass) varied significantly both within and among plots. The height, H:D and biomass of trees were positively correlated with annual precipitation and fragment area.

Conclusions: The association between forest structure and precipitation indicates that these forests plots are likely to be vulnerable to dry season intensification anticipated for the southern edge of the Amazon. Additionally, the reduction in the fragment area may contribute to reductions in forest biomass and tree height, and consequently ecosystem carbon stocks. Given the likely susceptibility of these forests, urgent conservation action is needed to prevent further habitat degradation.     

Genomics, environmental genomics and the issue of microbial species

A microbial species concept is crucial for interpreting the variation detected by genomics and environmental genomics among cultivated microorganisms and within natural microbial populations. Comparative genomic analyses of prokaryotic species as they are presently described and named have led to the provocative idea that prokaryotes may not form species as we think about them for plants and animals. There are good reasons to doubt whether presently recognized prokaryotic species are truly species. To achieve a better understanding of microbial species, we believe it is necessary to (i) re-evaluate traditional approaches in light of evolutionary and ecological theory, (ii) consider that different microbial species may have evolved in different ways and (iii) integrate genomic, metagenomic and genome-wide expression approaches with ecological and evolutionary theory. Here, we outline how we are using genomic methods to (i) identify ecologically distinct populations (ecotypes) predicted by theory to be species-like fundamental units of microbial communities, and (ii) test their species-like character through in situ distribution and gene expression studies. By comparing metagenomic sequences obtained from well-studied hot spring cyanobacterial mats with genomic sequences of two cultivated cyanobacterial ecotypes, closely related to predominant native populations, we can conduct in situ population genetics studies that identify putative ecotypes and functional genes that determine the ecotypes' ecological distinctness. If individuals within microbial communities are found to be grouped into ecologically distinct, species-like populations, knowing about such populations should guide us to a better understanding of how genomic variation is linked to community function.     

Exploring genomic variation associated with drought stress in Picea mariana populations

Predicted increases in drought and heat stress will likely induce shifts in species bioclimatic envelopes. Genetic variants adapted to water limitation may prove pivotal for species response under scenarios of increasing drought. In this study, we aimed to explore this hypothesis by investigating genetic variation in 16 populations of black spruce (Picea mariana) in relation to climate variables in Alaska. A total of 520 single nucleotide polymorphisms (SNPs) were genotyped for 158 trees sampled from areas of contrasting climate regimes. We used multivariate and univariate genotype‐by‐environment approaches along with available gene annotations to investigate the relationship between climate and genetic variation among sampled populations. Nine SNPs were identified as having a significant association with climate, of which five were related to drought stress response. Outlier SNPs with respect to the overall environment were significantly overrepresented for several biological functions relevant for coping with variable hydric regimes, including osmotic stress response. This genomic imprint is consistent with local adaptation of black spruce to drought stress. These results suggest that natural selection acting on standing variation prompts local adaptation in forest stands facing water limitation. Improved understanding of possible adaptive responses could inform our projections about future forest dynamics and help prioritize populations that harbor valuable genetic diversity for conservation.     

How mass spectrometric approaches applied to bacterial identification have revolutionized the study of human gut microbiota

Introduction: Describing the human hut gut microbiota is one the most exciting challenges of the 21^st century. Currently, high-throughput sequencing methods are considered as the gold standard for this purpose, however, they suffer from several drawbacks, including their inability to detect minority populations. The advent of mass-spectrometric (MS) approaches to identify cultured bacteria in clinical microbiology enabled the creation of the culturomics approach, which aims to establish a comprehensive repertoire of cultured prokaryotes from human specimens using extensive culture conditions.

Areas covered: This review first underlines how mass spectrometric approaches have revolutionized clinical microbiology. It then highlights the contribution of MS-based methods to culturomics studies, paying particular attention to the extension of the human gut microbiota repertoire through the discovery of new bacterial species.

Expert commentary: MS-based approaches have enabled cultivation methods to be resuscitated to study the human gut microbiota and thus to fill in the blanks left by high-throughput sequencing methods in terms of culturing minority populations. Continued efforts to recover new taxa using culture methods, combined with their rapid implementation in genomic databases, would allow for an exhaustive analysis of the gut microbiota through the use of a comprehensive approach.     

Utility of closely related taxa for genetic studies of adaptive variation and speciation: Current state and perspectives in plants with focus on forest tree species

Studies of adaptation and speciation have greatly benefited from rapid progress of DNA sequencing and genotyping technologies. Comparative genomics of closely related taxa has great potential to advance evolutionary research on genetic architecture of adaptive traits and reproductive isolation. Such studies that utilized closely related plant species and ecotypes have already provided some important insights into genomic regions and/or genes that are potentially involved in local adaptation and speciation. The choice of an appropriate species model for such research is crucial. The paper discusses current approaches used to reveal the patterns of intra‐ and interspecific divergence due to natural selection. Its outcomes in herbaceous plants and forest trees are briefly summarized and compared to reveal general regularities concerning evolutionary processes. We then highlight the importance of multispecies studies and discuss the utility of several related pine taxa as fine candidates for evolutionary inferences. Genetically similar but ecologically and phenotypically diverged taxa seem a promising study system to search for genomic patterns of speciation and adaptive variation.     

Disturbances catalyze the adaptation of forest ecosystems to changing climate conditions

The rates of anthropogenic climate change substantially exceed those at which forest ecosystems – dominated by immobile, long‐lived organisms – are able to adapt. The resulting maladaptation of forests has potentially detrimental effects on ecosystem functioning. Furthermore, as many forest‐dwelling species are highly dependent on the prevailing tree species, a delayed response of the latter to a changing climate can contribute to an extinction debt and mask climate‐induced biodiversity loss. However, climate change will likely also intensify forest disturbances. Here, we tested the hypothesis that disturbances foster the reorganization of ecosystems and catalyze the adaptation of forest composition to climate change. Our specific objectives were (i) to quantify the rate of autonomous forest adaptation to climate change, (ii) examine the role of disturbance in the adaptation process, and (iii) investigate spatial differences in climate‐induced species turnover in an unmanaged mountain forest landscape (Kalkalpen National Park, Austria). Simulations with a process‐based forest landscape model were performed for 36 unique combinations of climate and disturbance scenarios over 1000 years. We found that climate change strongly favored European beech and oak species (currently prevailing in mid‐ to low‐elevation areas), with novel species associations emerging on the landscape. Yet, it took between 357 and 706 years before the landscape attained a dynamic equilibrium with the climate system. Disturbances generally catalyzed adaptation and decreased the time needed to attain equilibrium by up to 211 years. However, while increasing disturbance frequency and severity accelerated adaptation, increasing disturbance size had the opposite effect. Spatial analyses suggest that particularly the lowest and highest elevation areas will be hotspots of future species change. We conclude that the growing maladaptation of forests to climate and the long lead times of autonomous adaptation need to be considered more explicitly in the ongoing efforts to safeguard biodiversity and ecosystem services provisioning.