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Abstract Stomata play a critical role in regulating plant responses to climate. Where sister species differ in stomatal traits, interspecific gene flow can influence the evolutionary trajectory of trait variation, with consequences to adaptation.Leveraging six latitudinally-distributed transects spanning the natural hybrid zone betweenPopulus trichocarpa–P. balsamifera, we used whole genome resequencing and replicate common garden experiments to test the role that interspecific gene flow and selection play to stomatal trait evolution.While species-specific differences in the distribution of stomata persist betweenP. balsamiferaandP. trichocarpa, hybrids on average resembledP. trichocarpa. Admixture mapping identified several candidate genes associated with stomatal trait variation in hybrids includingTWIST, a homolog ofSPEECHLESSinArabidopsis, that initiates stomatal development via asymmetric cell divisions. Geographic clines revealed candidate genes deviating from genome-wide average patterns of introgression, suggesting restricted gene flow and the maintenance of adaptive differences. Climate associations, particularly with precipitation, indicated selection shapes local ancestry at candidate genes across transects.These results highlight the role of climate in shaping stomatal trait evolution inPopulusand demonstrate how interspecific gene flow creates novel genetic combinations that may enhance adaptive potential in changing environments. 

Abstract Co-adaptation of cytoplasmic and nuclear genomes are critical to physiological function for many species. Despite this understanding, hybridization can disrupt co-adaptation leading to a mismatch between maternally-inherited cytoplasmic genomes and biparentally inherited nuclear genomes. Few studies have examined the consequences of cytonuclear interactions to physiological function across environments. Here, we quantify the degree of co-introgression between chloroplast and nuclear-chloroplast (N-cp) genes across repeated hybrid zones and its consequences to physiological function across environments. We use whole-genome resequencing and common garden experiments with clonally replicated genotypes sampled across the natural hybrid zone betweenPopulus trichocarpaandP. balsamifera. We use geographic clines to test for co-introgression of the chloroplast genome with N-cp and non-interacting nuclear genes. Co-introgression of chloroplast and N-cp genes was limited although contact zone-specific patterns suggest that local environments may influence co-introgression. Combining ancestry estimates with phenotypic data across common gardens revealed that mismatches between chloroplast and nuclear ancestry can influence physiological performance, but the strength and direction of these effects vary depending on the environment. Overall, this study highlights the importance of cytonuclear interactions to adaptation, and the role of environment in modifying the effect of those interactions. 

Abstract In a rapidly changing environment, predicting changes in the growth and survival of local populations can inform conservation and management. Plastic responses vary as a result of genetic differentiation within and among species, so accurate rangewide predictions require characterization of genotype-specific reaction norms across the continuum of historic and future climate conditions comprising a species’ range. Natural hybrid zones can give rise to novel recombinant genotypes associated with high phenotypic variability, further increasing the variance of plastic responses within the ranges of the hybridizing species. Experiments that plant replicated genotypes across a range of environments can characterize genotype-specific reaction norms; identify genetic, geographic, and climatic factors affecting variation in climate responses; and make predictions of climate responses across complex genetic and geographic landscapes. The North American hybrid zone ofPopulus trichocarpaandP. balsamiferarepresents a natural system in which reaction norms are likely to vary with underlying genetic variation that has been shaped by climate, geography, and introgression. Here, we leverage a dataset containing 45 clonal genotypes of varying ancestry from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range, including sites warmer than the natural species ranges. Growth and mortality were measured over two years, enabling us to model reaction norms for each genotype across these tested environments. Genomic variation associated with species ancestry and northern/southern regions significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade-off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with moreP. trichocarpaancestry may gain an advantage under warmer climates. Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape-level effects. 

Summary Plastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype‐specific reaction norms across the continuum of historic and future climate conditions comprising a species' range.The North American hybrid zone ofPopulus trichocarpaandPopulus balsamiferarepresents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 44 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over 2 yr, enabling us to model reaction norms for each genotype across these tested environments.Species ancestry and intraspecific genomic variation significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade‐off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with moreP. trichocarpaancestry may gain an advantage under warmer climates.Spatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape‐level effects. 

Shifting range limits are predicted for many species as the climate warms. However, the rapid pace of climate change will challenge the natural dispersal capacity of long-lived, sessile organisms such as forest trees. Adaptive responses of populations will, therefore, depend on levels of genetic variation and plasticity for climate-responsive traits, which likely vary across the range due to expansion history and current patterns of selection. Here, we study levels of genetic and plastic variation for phenology and growth traits in populations of red spruce ( Picea rubens ), from the range core to the highly fragmented trailing edge. We measured more than 5000 offspring sampled from three genetically distinct regions (core, margin and edge) grown in three common gardens replicated along a latitudinal gradient. Genetic variation in phenology and growth showed low to moderate heritability and differentiation among regions, suggesting some potential to respond to selection. Phenology traits were highly plastic, but this plasticity was generally neutral or maladaptive in the effect on growth, revealing a potential liability under warmer climates. These results suggest future climate adaptation will depend on the regional availability of genetic variation in red spruce and provide a resource for the design and management of assisted gene flow. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’. 

Red spruce (Picea rubens Sarg.) is a coniferous tree with a highly fragmented range in eastern North American montane forests. It serves as a foundational species for many locally rare and threatened taxa and has therefore been the focus of large-scale reforestation efforts aimed at restoring these montane ecosystems, yet genetic input guiding these efforts has been lacking. To tackle this issue, we took advantage of a common garden experiment and a whole exome sequencing dataset to investigate the impact of different population genetic parameters on early-life seedling fitness in red spruce. The level of inbreeding, genetic diversity and genetic load were assessed for 340 mother trees sampled from 65 localities across the spe- cies range and compared to different fitness traits measured on 5100 of their seedlings grown in a controlled environment. We identified an overall positive influence of genetic diversity and negative impact of genetic load and population-level inbreeding on early-life fitness. Those associations were most apparent for the highly fragmented populations in the Central and Southern Appalachians, where lower genetic diversity and higher inbreeding were associated with lower germination rate, shorter height and reduced early-life fitness of the seedlings. These results provide unprecedented information that could be used by field managers aiming to restore red spruce forests and to maximize the success of future plantations. 

Signals of local adaptation have been found in many plants and animals, highlighting the heterogeneity in the distribution of adaptive genetic variation throughout species ranges. In the coming decades, global climate change is expected to induce shifts in the selective pressures that shape this adaptive variation. These changes in selective pressures will likely result in varying degrees of local climate maladaptation and spatial reshuffling of the underlying distributions of adaptive alleles. There is a growing interest in using population genomic data to help predict future disruptions to locally adaptive gene-environment associations. One motivation behind such work is to better understand how the effects of changing climate on populations’ short-term fitness could vary spatially across species ranges. Here we review the current use of genomic data to predict the disruption of local adaptation across current and future climates. After assessing goals and motivations underlying the approach, we review the main steps and associated statistical methods currently in use and explore our current understanding of the limits and future potential of using genomics to predict climate change (mal)adaptation. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 51 is November 2, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates. 

Droughts of increasing severity and frequency are a primary cause of forest mortality associated with climate change. Yet, fundamental knowledge gaps regarding the complex physiology of trees limit the development of more effective management strategies to mitigate drought effects on forests. Here, we highlight some of the basic research needed to better understand tree drought physiology and how new technologies and interdisciplinary approaches can be used to address them. Our discussion focuses on how trees change wood development to mitigate water stress, hormonal responses to drought, genetic variation underlying adaptive drought phenotypes, how trees ‘remember’ prior stress exposure, and how symbiotic soil microbes affect drought response. Next, we identify opportunities for using research findings to enhance or develop new strategies for managing drought effects on forests, ranging from matching genotypes to environments, to enhancing seedling resilience through nursery treatments, to landscape‐scale monitoring and predictions. We conclude with a discussion of the need for co‐producing research with land managers and extending research to forests in critical ecological regions beyond the temperate zone. 

Summary Local adaptation to climate is common in plant species and has been studied in a range of contexts, from improving crop yields to predicting population maladaptation to future conditions. The genomic era has brought new tools to study this process, which was historically explored through common garden experiments.In this study, we combine genomic methods and common gardens to investigate local adaptation in red spruce and identify environmental gradients and loci involved in climate adaptation. We first use climate transfer functions to estimate the impact of climate change on seedling performance in three common gardens. We then explore the use of multivariate gene–environment association methods to identify genes underlying climate adaptation, with particular attention to the implications of conducting genome scans with and without correction for neutral population structure.This integrative approach uncovered phenotypic evidence of local adaptation to climate and identified a set of putatively adaptive genes, some of which are involved in three main adaptive pathways found in other temperate and boreal coniferous species: drought tolerance, cold hardiness, and phenology. These putatively adaptive genes segregated into two ‘modules’ associated with different environmental gradients.This study nicely exemplifies the multivariate dimension of adaptation to climate in trees.