Identifying genetic variation associated with environmental gradients and drought-tolerance phenotypes in ponderosa pine.

As climate changes, understanding the genetic basis of local adaptation in plants becomes an ever more pressing issue. Combining genotype-environment association (GEA) with genotype-phenotype association (GPA) analysis has an exciting potential to uncover the genetic basis of environmental responses. We use these approaches to identify genetic variants linked to local adaptation to drought in Pinus ponderosa. Over 4 million Single Nucleotide Polymorphisms (SNPs) were identified using 223 individuals from across the Sierra Nevada of California. 927,740 (22.3%) SNPs were retained after filtering for proximity to genes and used in our association analyses. We found 1374 associated with five major climate variables, with the largest number (1151) associated with April 1st snowpack. We also conducted a greenhouse study with various drought-tolerance traits measured in first-year seedlings of a subset of the genotyped trees grown in the greenhouse. 796 SNPs were associated with control-condition trait values, while 1149 were associated with responsiveness of these traits to drought. While no individual SNPs were associated with both the environmental variables and the measured traits, several annotated genes were associated with both, particularly those involved in cell wall formation, biotic and abiotic stress responses, and ubiquitination. However, the functions of many of the associated genes have not yet been determined due to the lack of gene annotation information for conifers. Future studies are needed to assess the developmental roles and ecological significance of these unknown genes.

Simulating the effects of local adaptation and life history on the ability of plants to track climate shifts.

Many studies have examined the impact of dispersal on local adaptation, but much less attention has been paid to how local adaptation influences range shifts. The aim of this study was to test how local adaptation might affect climate-driven range shifts in plants, and if this might differ between plants with different life histories. Simulated range shift dynamics were compared for hypothetical annual, perennial and tree species, each comprised of either one plastic genotype or six locally adapted genotypes. The landscape consists of shifting climate bands made up of 20 × 20 m patches containing multiple individuals. Effects of seed dispersal, breadth of the plastic species' tolerance, steepness of the climate gradient and rate of the climate shift are also examined. Local adaptation increased the equilibrium range size and aided range shifts by boosting fitness near range edges. However, when the rate of climate change was doubled on a steep gradient, locally adapted trees exhibited a higher percent loss of range during the climate shift. The plastic annual species with short dispersal was unable to recover its range size even after the climate stabilized, while the locally adapted annuals tracked climate change well. The results suggest that in most situations local adaptation and longer dispersal distances will be advantageous, though not necessarily sufficient, for tracking suitable climates. However, local adaptation might put species with long generation times at greater risk when climate shifts are very rapid. If confirmed by empirical tests, these results suggest that identifying variation between species in how fitness varies along climate gradients and in these key demographic rates might aid in prioritizing management actions.

Fight or flight? Potential tradeoffs between drought defense and reproduction in conifers.

Plants frequently exhibit tradeoffs between reproduction and growth when resources are limited, and often change these allocation patterns in response to stress. Shorter-lived plants such as annuals tend to allocate relatively more resources toward reproduction when stressed, while longer-lived plants tend to invest more heavily in survival and stress defense. However, severe stress may affect the fitness implications of allocating relatively more resources to reproduction versus stress defense. Increased drought intensity and duration have led to widespread mortality events in coniferous forests. In this review, we ask how potential tradeoffs between reproduction and survival influence the likelihood of drought-induced mortality and species persistence. We propose that trees may exhibit what we call 'fight or flight' behaviors under stress. 'Fight' behaviors involve greater resource allocation toward survival (e.g., growth, drought-resistant xylem and pest defense). 'Flight' consists of higher relative allocation of resources to reproduction, potentially increasing both offspring production and mortality risk for the adult. We hypothesize that flight behaviors increase as drought stress escalates the likelihood of mortality in a given location.

Population genetics and adaptation to climate along elevation gradients in invasive Solidago canadensis.

Gene flow between populations may either support local adaptation by supplying genetic variation on which selection may act, or counteract it if maladapted alleles arrive faster than can be purged by selection. Although both such effects have been documented within plant species' native ranges, how the balance of these forces influences local adaptation in invasive plant populations is less clear, in part because introduced species often have lower genetic variation initially but also tend to have good dispersal abilities. To evaluate the extent of gene flow and adaptation to local climate in invasive populations of Solidago canadensis, and the implications of this for range expansion, we compared population differentiation at microsatellite and chloroplast loci for populations across Switzerland and assessed the effect of environmental transfer distance using common gardens. We found that while patterns of differentiation at neutral genetic markers suggested that populations are connected through extensive pollen and seed movement, common-garden plants nonetheless exhibited modest adaptation to local climate conditions. Growth rate and flower production declined with climatic distance from a plant's home site, with clones from colder home sites performing better at or above the range limit. Such adaptation in invasive species is likely to promote further spread, particularly under climate change, as the genotypes positioned near the range edge may be best able to take advantage of lengthening growing seasons to expand the range.

Intraspecific trait variation across scales: implications for understanding global change responses.

Recognition of the importance of intraspecific variation in ecological processes has been growing, but empirical studies and models of global change have only begun to address this issue in detail. This review discusses sources and patterns of intraspecific trait variation and their consequences for understanding how ecological processes and patterns will respond to global change. We examine how current ecological models and theories incorporate intraspecific variation, review existing data sources that could help parameterize models that account for intraspecific variation in global change predictions, and discuss new data that may be needed. We provide guidelines on when it is most important to consider intraspecific variation, such as when trait variation is heritable or when nonlinear relationships are involved. We also highlight benefits and limitations of different model types and argue that many common modeling approaches such as matrix population models or global dynamic vegetation models can allow a stronger consideration of intraspecific trait variation if the necessary data are available. We recommend that existing data need to be made more accessible, though in some cases, new experiments are needed to disentangle causes of variation.

Simulating the Interacting Effects of Intraspecific Variation, Disturbance, and Competition on Climate-Driven Range Shifts in Trees.

Climate change is expected to favor shifts in plant distributions; some such shifts are already being observed along elevation gradients. However, the rate of such shifts may be limited by their ability to reach newly suitable areas and by competition from resident species. The degree of local adaptation and genetic variation may also play a role in the interaction between migrants and residents by affecting relative fitness. We used a simulation model to explore the interacting effects of dispersal, fecundity, disturbance, and genetic variation on range-edge dynamics between a pair of demographically similar tree species. Ideal climate for an individual is determined by genotype. The simulated landscape undergoes an 80-year period of climate change in which climate bands shift upslope; subsequently, climate is held constant for 300 years. The presence of a high-elevation competitor caused a significant lag in the range shift of the low-elevation species relative to competition-free scenarios. Increases in fecundity and dispersal distance both helped to speed up the replacement of the high-elevation species by the low-elevation species at their range boundary. While some disturbance scenarios facilitated this transition, frequent canopy disturbance inhibited colonization by removing reproductive adults and led to range contractions in both species. Differences between dispersal scenarios were more pronounced when disturbance was frequent (15 vs. 25 year return interval) and dispersal was limited. When the high-elevation species lacked genetic variation, its range was more-easily invaded by the low-elevation species, while a similar lack of variation in the low-elevation species inhibited colonization-but only when this lack of variation decreased the fitness of the affected species near the range boundary. Our model results support the importance of measuring and including dispersal/fecundity, disturbance type and frequency, and genetic variation when assessing the potential for range shifts and species vulnerability to climate change.

Evolutionary responses to global change: lessons from invasive species.

Biologists have recently devoted increasing attention to the role of rapid evolution in species' responses to environmental change. However, it is still unclear what evolutionary responses should be expected, at what rates, and whether evolution will save populations at risk of extinction. The potential of biological invasions to provide useful insights has barely been realised, despite the close analogies to species responding to global change, particularly climate change; in both cases, populations encounter novel climatic and biotic selection pressures, with expected evolutionary responses occurring over similar timescales. However, the analogy is not perfect, and invasive species are perhaps best used as an upper bound on expected change. In this article, we review what invasive species can and cannot teach us about likely evolutionary responses to global change and the constraints on those responses. We also discuss the limitations of invasive species as a model and outline directions for future research.

Can elevated CO2 and ozone shift the genetic composition of aspen (Populus tremuloides) stands?

The world's forests are currently exposed to increasing concentrations of carbon dioxide (CO2) and ozone (O3). Both pollutants can potentially exert a selective effect on plant populations. This, in turn, may lead to changes in ecosystem properties, such as carbon sequestration. Here, we report how elevated CO2 and O3 affect the genetic composition of a woody plant population via altered survival. Using data from the Aspen free-air CO2 enrichment (FACE) experiment (in which aspen clones were grown in factorial combinations of CO2 and O3), we develop a hierarchical Bayesian model of survival. We also examine how survival differences between clones could affect pollutant responses in the next generation. Our model predicts that the relative abundance of the tested clones, given equal initial abundance, would shift under either elevated CO2 or O3 as a result of changing survival rates. Survival was strongly affected by between-clone differences in growth responses. Selection could noticeably decrease O3 sensitivity in the next generation, depending on the heritability of growth responses and the distribution of seed production. The response to selection by CO2, however, is likely to be small. Our results suggest that the changing atmospheric composition could shift the genotypic composition and average pollutant responses of tree populations over moderate timescales.

Effects of plant genotype and insect dispersal rate on the population dynamics of a forest pest.

It has been shown that plant genotype can strongly affect not only individual herbivore performance, but also community composition and ecosystem function. Few studies, however, have addressed how plant genotype affects herbivore population dynamics. In this paper, we used a simulation modeling approach to ask how the genetic composition of a forest influences pest outbreak dynamics, using the example of aspen (Populus tremuloides) and forest tent caterpillars (FTC; Malacosoma disstria). Specifically, we examined how plant genotype, the relative size of genotypic patches, and the rate of insect dispersal between them, affect the frequency, amplitude, and duration of outbreaks. We found that coupling two different genotypes does not necessarily result in an averaging of insect dynamics. Instead, depending on the ratio of patch sizes, when dispersal rates are moderate, outbreaks in the two-genotype case may be more or less severe than in forests of either genotype alone. Thresholds for different dynamic behaviors were similar for all genotypic combinations. Thus, the qualitative behavior of a stand of two different genotypes can be predicted based on the response of the insect to each genotype, the relative sizes of the two patches, and the scale of insect dispersal.

Causes and consequences of unequal seedling production in forest trees: a case study in red oaks.

Inequality in reproductive success has important implications for ecological and evolutionary dynamics, but lifetime reproductive success is challenging to measure in long-lived species such as forest trees. While seed production is often used as a proxy for overall reproductive success, high mortality of seeds and the potential for trade-offs between seed number and quality draw this assumption into question. Parentage analyses of established seedlings can bring us one step closer to understanding the causes and consequences of variation in reproductive success. In this paper we demonstrate a new method for estimating individual seedling production and average percentage germination, using data from two mixed-species populations of red oaks (Quercus rubra, Q. velutina, Q. falcata, and Q. coccinea). We use these estimates to examine the distribution of female reproductive success and to test the relationship between seedling number and individual seed production, age, and growth rate. We show that both seed and seedling production are highly skewed, roughly conforming to zero-inflated lognormal distributions, rather than to the Poisson or negative-binomial distributions often assumed by population genetics analyses. While the number of established offspring is positively associated with mean annual seed production, a lower proportion of seeds from highly fecund individuals become seedlings. Our red oak populations also show evidence of trade-offs between growth rate and reproductive success. The high degree of inequality in seedling production shown here for red oaks, and by previous studies in other species, suggests that many trees may be more vulnerable to genetic drift than previously thought, if immigration in limited by fragmentation or other environmental changes.

Between-site differences in the scale of dispersal and gene flow in red oak.

BACKGROUND: Nut-bearing trees, including oaks (Quercus spp.), are considered to be highly dispersal limited, leading to concerns about their ability to colonize new sites or migrate in response to climate change. However, estimating seed dispersal is challenging in species that are secondarily dispersed by animals, and differences in disperser abundance or behavior could lead to large spatio-temporal variation in dispersal ability. Parentage and dispersal analyses combining genetic and ecological data provide accurate estimates of current dispersal, while spatial genetic structure (SGS) can shed light on past patterns of dispersal and establishment. METHODOLOGY AND PRINCIPAL FINDINGS: In this study, we estimate seed and pollen dispersal and parentage for two mixed-species red oak populations using a hierarchical bayesian approach. We compare these results to those of a genetic ML parentage model. We also test whether observed patterns of SGS in three size cohorts are consistent with known site history and current dispersal patterns. We find that, while pollen dispersal is extensive at both sites, the scale of seed dispersal differs substantially. Parentage results differ between models due to additional data included in bayesian model and differing genotyping error assumptions, but both indicate between-site dispersal differences. Patterns of SGS in large adults, small adults, and seedlings are consistent with known site history (farmed vs. selectively harvested), and with long-term differences in seed dispersal. This difference is consistent with predator/disperser satiation due to higher acorn production at the low-dispersal site. While this site-to-site variation results in substantial differences in asymptotic spread rates, dispersal for both sites is substantially lower than required to track latitudinal temperature shifts. CONCLUSIONS: Animal-dispersed trees can exhibit considerable spatial variation in seed dispersal, although patterns may be surprisingly constant over time. However, even under favorable conditions, migration in heavy-seeded species is likely to lag contemporary climate change.

Genetic evidence for hybridization in red oaks (Quercus sect. Lobatae, Fagaceae).

PREMISE OF THE STUDY: Hybridization is pervasive in many plant taxa, with consequences for species taxonomy, local adaptation, and management. Oaks (Quercus spp.) are thought to hybridize readily yet retain distinct traits, drawing into question the biological species concept for such taxa, but the true extent of gene flow is controversial. Genetic data are beginning to shed new light on this issue, but red oaks (section Lobatae), an important component of North American forests, have largely been neglected. Moreover, gene flow estimates may be sensitive to the choice of life stage, marker type, or genetic structure statistic. METHODS: We coupled genetic structure data with parentage analyses for two mixed-species stands in North Carolina. Genetic structure analyses of adults (including F(ST), R(ST), G'(ST), and structure) reflect long-term patterns of gene flow, while the percentage of seedlings with parents of two different species reflect current levels of gene flow. KEY RESULTS: Genetic structure analyses revealed low differentiation in microsatellite allele frequencies between co-occurring species, suggesting past gene flow. However, methods differed in their sensitivity to differentiation, indicating a need for caution when drawing conclusions from a single method. Parentage analyses identified >20% of seedlings as potential hybrids. The species examined exhibit distinct morphologies, suggesting selection against intermediate phenotypes. CONCLUSIONS: Our results suggest that hybridization between co-occurring red oaks occurs, but that selection may limit introgression, especially at functional loci. However, by providing a source of genetic variation, hybridization could influence the response of oaks and other hybridizing taxa to environmental change.

Estimating seed and pollen movement in a monoecious plant: a hierarchical Bayesian approach integrating genetic and ecological data.

The scale of seed and pollen movement in plants has a critical influence on population dynamics and interspecific interactions, as well as on their capacity to respond to environmental change through migration or local adaptation. However, dispersal can be challenging to quantify. Here, we present a Bayesian model that integrates genetic and ecological data to simultaneously estimate effective seed and pollen dispersal parameters and the parentage of sampled seedlings. This model is the first developed for monoecious plants that accounts for genotyping error and treats dispersal from within and beyond a plot in a fully consistent manner. The flexible Bayesian framework allows the incorporation of a variety of ecological variables, including individual variation in seed production, as well as multiple sources of uncertainty. We illustrate the method using data from a mixed population of red oak (Quercus rubra, Q. velutina, Q. falcata) in the NC piedmont. For simulated test data sets, the model successfully recovered the simulated dispersal parameters and pedigrees. Pollen dispersal in the example population was extensive, with an average father-mother distance of 178 m. Estimated seed dispersal distances at the piedmont site were substantially longer than previous estimates based on seed-trap data (average 128 m vs. 9.3 m), suggesting that, under some circumstances, oaks may be less dispersal-limited than is commonly thought, with a greater potential for range shifts in response to climate change.

A predictive framework to understand forest responses to global change.

Forests are one of Earth's critical biomes. They have been shown to respond strongly to many of the drivers that are predicted to change natural systems over this century, including climate, introduced species, and other anthropogenic influences. Predicting how different tree species might respond to this complex of forces remains a daunting challenge for forest ecologists. Yet shifts in species composition and abundance can radically influence hydrological and atmospheric systems, plant and animal ranges, and human populations, making this challenge an important one to address. Forest ecologists have gathered a great deal of data over the past decades and are now using novel quantitative and computational tools to translate those data into predictions about the fate of forests. Here, after a brief review of the threats to forests over the next century, one of the more promising approaches to making ecological predictions is described: using hierarchical Bayesian methods to model forest demography and simulating future forests from those models. This approach captures complex processes, such as seed dispersal and mortality, and incorporates uncertainty due to unknown mechanisms, data problems, and parameter uncertainty. After describing the approach, an example by simulating drought for a southeastern forest is offered. Finally, there is a discussion of how this approach and others need to be cast within a framework of prediction that strives to answer the important questions posed to environmental scientists, but does so with a respect for the challenges inherent in predicting the future of a complex biological system.