Sally N. Aitken

Adaptation, migration or extirpation: climate change outcomes for tree populations

Species distribution models predict a wholesale redistribution of trees in the next century, yet migratory responses necessary to spatially track climates far exceed maximum post‐glacial rates. The extent to which populations will adapt will depend upon phenotypic variation, strength of selection, fecundity, interspecific competition, and biotic interactions. Populations of temperate and boreal trees show moderate to strong clines in phenology and growth along temperature gradients, indicating substantial local adaptation. Traits involved in local adaptation appear to be the product of small effects of many genes, and the resulting genotypic redundancy combined with high fecundity may facilitate rapid local adaptation despite high gene flow. Gene flow with preadapted alleles from warmer climates may promote adaptation and migration at the leading edge, while populations at the rear will likely face extirpation. Widespread species with large populations and high fecundity are likely to persist and adapt, but will likely suffer adaptational lag for a few generations. As all tree species will be suffering lags, interspecific competition may weaken, facilitating persistence under suboptimal conditions. Species with small populations, fragmented ranges, low fecundity, or suffering declines due to introduced insects or diseases should be candidates for facilitated migration.

Potential for evolutionary responses to climate change – evidence from tree populations

Evolutionary responses are required for tree populations to be able to track climate change. Results of 250 years of common garden experiments show that most forest trees have evolved local adaptation, as evidenced by the adaptive differentiation of populations in quantitative traits, reflecting environmental conditions of population origins. On the basis of the patterns of quantitative variation for 19 adaptation-related traits studied in 59 tree species (mostly temperate and boreal species from the Northern hemisphere), we found that genetic differentiation between populations and clinal variation along environmental gradients were very common (respectively, 90% and 78% of cases). Thus, responding to climate change will likely require that the quantitative traits of populations again match their environments. We examine what kind of information is needed for evaluating the potential to respond, and what information is already available. We review the genetic models related to selection responses, and what is known currently about the genetic basis of the traits. We address special problems to be found at the range margins, and highlight the need for more modeling to understand specific issues at southern and northern margins. We need new common garden experiments for less known species. For extensively studied species, new experiments are needed outside the current ranges. Improving genomic information will allow better prediction of responses. Competitive and other interactions within species and interactions between species deserve more consideration. Despite the long generation times, the strong background in quantitative genetics and growing genomic resources make forest trees useful species for climate change research. The greatest adaptive response is expected when populations are large, have high genetic variability, selection is strong, and there is ecological opportunity for establishment of better adapted genotypes.

Evolutionary and plastic responses to climate change in terrestrial plant populations

As climate change progresses, we are observing widespread changes in phenotypes in many plant populations. Whether these phenotypic changes are directly caused by climate change, and whether they result from phenotypic plasticity or evolution, are active areas of investigation. Here, we review terrestrial plant studies addressing these questions. Plastic and evolutionary responses to climate change are clearly occurring. Of the 38 studies that met our criteria for inclusion, all found plastic or evolutionary responses, with 26 studies showing both. These responses, however, may be insufficient to keep pace with climate change, as indicated by eight of 12 studies that examined this directly. There is also mixed evidence for whether evolutionary responses are adaptive, and whether they are directly caused by contemporary climatic changes. We discuss factors that will likely influence the extent of plastic and evolutionary responses, including patterns of environmental changes, species’ life history characteristics including generation time and breeding system, and degree and direction of gene flow. Future studies with standardized methodologies, especially those that use direct approaches assessing responses to climate change over time, and sharing of data through public databases, will facilitate better predictions of the capacity for plant populations to respond to rapid climate change.

Putting the landscape into the genomics of trees: approaches for understanding local adaptation and population responses to changing climate

The Forest ecosystem genomics Research: supporTing Transatlantic Cooperation project (FoResTTraC, http://www.foresttrac.eu/) sponsored a workshop in August 2010 to evaluate the potential for using a landscape genomics approach for studying plant adaptation to the environment and the potential of local populations for coping with changing climate. This paper summarizes our discussions and articulates a vision of how we believe forest trees offer an unparalleled opportunity to address fundamental biological questions, as well as how the application of landscape genomic methods complement to traditional forest genetic approaches that provide critical information needed for natural resource management. In this paper, we will cover four topics. First, we begin by defining landscape genomics and briefly reviewing the unique situation for tree species in the application of this approach toward understanding plant adaptation to the environment. Second, we review traditional approaches in forest genetics for studying local adaptation and identifying loci underlying locally adapted phenotypes. Third, we present existing and emerging methods available for landscape genomic analyses. Finally, we briefly touch on how these approaches can aid in understanding practical topics such as management of tree populations facing climate change.

Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis).

• Genecological studies in widespread tree species have revealed steep genetic clines along environmental gradients for climate-related traits. In a changing climate, the ecological and economic importance of conifers necessitates an appraisal of how molecular genetic variation shapes quantitative trait variation, and one of the most promising approaches to answer this question is association mapping. • We phenotyped a wide collection of 410 individuals of the widely distributed conifer Sitka spruce rangewide (Picea sitchensis) for budset timing and autumn cold hardiness, and genotyped these individuals for a panel of 768 single nucleotide polymorphisms (SNPs) representing > 200 expressed nuclear genes. • After correcting for population structure, associations were detected in 28 of the candidate genes, which cumulatively explained 28 and 34% of the phenotypic variance in cold hardiness and budset, respectively. Most notable among the associations were five genes putatively involved in light signal transduction, the key pathway regulating autumn growth cessation in perennials. Many SNPs with phenotypic associations were also correlated with at least one climate variable. • This study represents a significant step toward the goal of characterizing the genomic basis of adaptation to local climate in conifers, and provides an important resource for breeding and conservation genetics in a changing climate.

Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis)

Cold acclimation in conifers is a complex process, the timing and extent of which reflects local adaptation and varies widely along latitudinal gradients for many temperate and boreal tree species. Despite their ecological and economic importance, little is known about the global changes in gene expression that accompany autumn cold acclimation in conifers. Using three populations of Sitka spruce (Picea sitchensis) spanning the species range, and a Picea cDNA microarray with 21,840 unique elements, within- and among-population gene expression was monitored during the autumn. Microarray data were validated for selected genes using real-time PCR. Similar numbers of genes were significantly twofold upregulated (1257) and downregulated (967) between late summer and early winter. Among those upregulated were dehydrins, pathogenesis-related/antifreeze genes, carbohydrate and lipid metabolism genes, and genes involved in signal transduction and transcriptional regulation. Among-population microarray hybridizations at early and late autumn time points revealed substantial variation in the autumn transcriptome, some of which may reflect local adaptation. These results demonstrate the complexity of cold acclimation in conifers, highlight similarities and differences to cold tolerance in annual plants, and provide a solid foundation for functional and genetic studies of this important adaptive process.

Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis

Fossil pollen records suggest rapid migration of tree species in response to Quaternary climate warming. Long-distance dispersal and high gene flow would facilitate rapid migration, but would initially homogenize variation among populations. However, contemporary clinal variation in adaptive traits along environmental gradients shown in many tree species suggests that local adaptation can occur during rapid migration over just a few generations in interglacial periods. In this study, we compared growth performance and pollen genetic structure among populations to investigate how populations of Sitka spruce (Picea sitchensis) have responded to local selection along the historical migration route. The results suggest strong adaptive divergence among populations (average QST=0.61), corresponding to climatic gradients. The population genetic structure, determined by microsatellite markers (RST=0.09; FST=0.11), was higher than previous estimates from less polymorphic genetic markers. The significant correlation between geographic and pollen haplotype genetic (RST) distances (r=0.73, P<0.01) indicates that the current genetic structure has been shaped by isolation-by-distance, and has developed in relatively few generations. This suggests relatively limited gene flow among populations on a recent timescale. Gene flow from neighboring populations may have provided genetic diversity to founder populations during rapid migration in the early stages of range expansion. Increased genetic diversity subsequently enhanced the efficiency of local selection, limiting gene flow primarily to among similar environments and facilitating the evolution of adaptive clinal variation along environmental gradients.

Whitebark pine (Pinus albicaulis) assisted migration potential: testing establishment north of the species range.

The translocation of species into habitable locations outside of their current ranges, termed assisted migration, has been proposed as a means of saving vulnerable species from extinction as a result of climate change. We explore the use of this controversial technique using a threatened keystone species in western North America, whitebark pine (Pinus albicaulis), as a case study. Species distribution models predict that whitebark pine will be extirpated from most of its current range as temperatures rise over the next 70 years. However, the same models indicate that a large area within northwestern British Columbia, Canada, is climatically suitable for the species under current conditions and will remain so throughout the 21st century. To test the capacity of whitebark pine to establish relative to climatic and habitat features within its predicted climatic range, we planted seeds from seven populations in eight locations spanning from 600 km southeast to 800 km northwest of the northern boundary of the current species range. During the first three growing seasons, germination occurred in all locations. Nearly three times as many treated (induced maturation and broken dormancy) than untreated seeds germinated, and most treated seeds germinated a year earlier than the untreated seeds. Germination, survival, and growth were primarily influenced by seed mass, site climate conditions related to the duration of snow cover, and provenance temperature. Our experiment provides a preliminary test of models predicting the existence of climatically suitable whitebark pine habitat north of the current species ranges. More broadly, our techniques and results inform the development of scientific guidelines for assisting the migration of other species that are highly threatened by climate change. Applied case studies of this kind are critical for assessing the utility of species distribution models as conservation planning tools.

Genecology and Gene Resource Management Strategies for Conifer Cold Hardiness

It has long been recognized that considerable genetic variation exists within conifer species for cold hardiness and associated phenological traits. As early as 1759, Linnaeus reported that yew trees from France were less cold hardy than local ones in Sweden (Hesselman 1907) and in 1881, von Seckendorff observed differences in cold hardiness between provenances of Abies douglasii Lindl. [syn. Pseudotsuga menziesii (Mirb.) Franco] from Canada (summarized by Langlet 1971). Since these early observations, clinal patterns of variation have been documented at both relatively coarse and fine spatial scales, and some broad generalizations can be drawn from the extensive literature.

Strong spatial genetic structure in peripheral but not core populations of Sitka spruce [Picea sitchensis (Bong.) Carr.]

We examined spatial genetic structure within eight populations of Sitka spruce classified as core or peripheral based on ecological niche, and continuous or disjunct based on species distribution. In each population, 200 trees were spatially mapped and genotyped for eight cDNA‐based sequence tagged site (STS) codominant markers. Spatial autocorrelation was assessed by estimating pij, the average co‐ancestry coefficient, between individuals within distance intervals. The distribution of alleles and genotypes within core populations was almost random, with nonsignificant co‐ancestry values among trees as close as 50 m in core populations. In contrast, the distribution of alleles and genotypes within peripheral populations revealed an aggregation of similar multilocus genotypes, with co‐ancestry values greater than 0.20 among trees up to 50 m apart and significant, positive values between trees up to 500 m. The relatively high density of reproductive adults in core populations may lead to highly overlapping seed shadows that limit development of spatial genetic structure. However, in peripheral populations with a lower density of adults, the distribution of alleles and genotypes was highly structured, likely due to offspring establishment near maternal trees and subsequent biparental inbreeding, as well as more recent population establishment at the leading edge of post‐Pleistocene range expansion. Conserving genetic diversity in peripheral populations may require larger reserves for in situ conservation than required in core populations. These data on spatial genetic structure can be used to provide guidance for sampling strategies for both ex situ conservation and research collections.