Parallel adaptation to climate above the 35th parallel

Independent or parallel evolution of similar traits is key to understanding the genetics and limitations of adaptation. Adaptation from the same genetic changes in different populations defines parallel evolution. Such genetic changes can derive from standing ancestral variation or de novo mutations and excludes instances of adaptive introgression. In this issue of Molecular Ecology, Walden et al.(2020) investigate the scale of parallel climate adaptation from standing genetic variation between two North American Arabidopsis lyrata lineages, each formed by a distinct evolutionary history during the last glacial cycle. By identifying adaptive variants correlated with three ecologically significant climatic gradients, they show that instead of the same genetic variants or even genes, parallel evolution is only observed at the level of biological processes. The evolution of independent adaptive variants to climate in two genetically close lineages is explained by their different post‐glacial demographic histories. Separate glacial refugia and strong population bottlenecks were probably sufficient to change the landscape of shared allele frequencies, hindering the possibility of parallel evolution.     

Evolutionary tracking is determined by differential selection on demographic rates and density dependence

Recent ecological forecasts predict that ~25% of species worldwide will go extinct by 2050. However, these estimates are primarily based on environmental changes alone and fail to incorporate important biological mechanisms such as genetic adaptation via evolution. Thus, environmental change can affect population dynamics in ways that classical frameworks can neither describe nor predict. Furthermore, often due to a lack of data, forecasting models commonly describe changes in population demography by summarizing changes in fecundity and survival concurrently with the intrinsic growth rate (r). This has been shown to be an oversimplification as the environment may impose selective pressure on specific demographic rates (birth and death) rather than directly on r (the difference between the birth and death rates). This differential pressure may alter population response to density, in each demographic rate, further diluting the information combined to produce r. Thus, when we consider the potential for persistence via adaptive evolution, populations with the same r can have different abilities to persist amidst environmental change. Therefore, we cannot adequately forecast population response to climate change without accounting for demography and selection on density dependence. Using a continuous‐time Markov chain model to describe the stochastic dynamics of the logistic model of population growth and allow for trait evolution via mutations arising during birth events, we find persistence via evolutionary tracking more likely when environmental change alters birth rather than the death rate. Furthermore, species that evolve responses to changes in the strength of density dependence due to environmental change are less vulnerable to extinction than species that undergo selection independent of population density. By incorporating these key demographic considerations into our predictive models, we can better understand how species will respond to climate change.     

Loci under selection during multiple range expansions of an invasive plant are mostly population specific,but patterns are associated with climate

Identifying the genes underlying rapid evolutionary changes, describing their function and ascertaining the environmental pressures that determine fitness are the central elements needed for understanding of evolutionary processes and phenotypic changes that improve the fitness of populations. It has been hypothesized that rapid adaptive changes in new environments may contribute to the rapid spread and success of invasive plants and animals. As yet, studies of adaptation during invasion are scarce, as is knowledge of the genes underlying adaptation, especially in multiple replicated invasions. Here, we quantified how genotype frequencies change during invasions, resulting in rapid evolution of naturalized populations. We used six fully replicated common garden experiments in Brazil where Pinus taeda (loblolly pine) was introduced at the same time, in the same numbers, from the same seed sources, and has formed naturalized populations expanding outward from the plantations. We used a combination of nonparametric, population genetics and multivariate statistics to detect changes in genotype frequencies along each of the six naturalization gradients and their association with climate as well as shifts in allele frequencies compared to the source populations. Results show 25 genes with significant shifts in genotype frequencies. Six genes had shifts in more than one population. Climate explained 25% of the variation in the groups of genes under selection across all locations, but specific genes under strong selection during invasions did not show climate‐related convergence. In conclusion, we detected rapid evolutionary changes during invasive range expansions, but the particular gene‐level patterns of evolution may be population specific.     

Plant adaptation to climate change—Where are we?

Climate change poses critical challenges for population persistence in natural communities, for agriculture and environmental sustainability, and for food security. In this review, we discuss recent progress in climatic adaptation in plants. We evaluate whether climate change exerts novel selection and disrupts local adaptation, whether gene flow can facilitate adaptive responses to climate change, and whether adaptive phenotypic plasticity could sustain populations in the short term. Furthermore, we discuss how climate change influences species interactions. Through a more in‐depth understanding of these eco‐evolutionary dynamics, we will increase our capacity to predict the adaptive potential of plants under climate change. In addition, we review studies that dissect the genetic basis of plant adaptation to climate change. Finally, we highlight key research gaps, ranging from validating gene function to elucidating molecular mechanisms, expanding research systems from model species to other natural species, testing the fitness consequences of alleles in natural environments, and designing multifactorial studies that more closely reflect the complex and interactive effects of multiple climate change factors. By leveraging interdisciplinary tools (e.g., cutting‐edge omics toolkits, novel ecological strategies, newly developed genome editing technology), researchers can more accurately predict the probability that species can persist through this rapid and intense period of environmental change, as well as cultivate crops to withstand climate change, and conserve biodiversity in natural systems.     

The phenomenology of niche evolution via quantitative traits in a 'black-hole' sink

Previous studies of adaptive evolution in sink habitats (in which isolated populations of a species cannot persist deterministically) have highlighted the importance of demographic constraints in slowing such evolution, and of immigration in facilitating adaptation. These studies have relied upon either single-locus models or deterministic quantitative genetic formulations. We use individual-based simulations to examine adaptive evolution in a 'black-hole' sink environment where fitness is governed by a polygenic character. The simulations track both the number of individuals and their multi-locus genotypes, and incorporate, in a natural manner, both demographic and genetic stochastic processes. In agreement with previous studies, our findings reveal the central parts played by demographic constraints and immigration in adaptation within a sink (adaptation is more difficult in environments with low absolute fitness, and higher immigration can accelerate adaptation). A novel finding is that there is a 'punctuational' pattern in adaptive evolution in sink environments. Populations typically stay maladapted for a long time, and then rapidly shift into a relatively adapted state, in which persistence no longer depends upon recurrent immigration.     

Evolutionary genetics of plant adaptation

Plants provide unique opportunities to study the mechanistic basis and evolutionary processes of adaptation to diverse environmental conditions. Complementary laboratory and field experiments are important for testing hypotheses reflecting long-term ecological and evolutionary history. For example, these approaches can infer whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy), where native alleles are best adapted to local conditions, or if local adaptation is caused by conditional neutrality at many loci, where alleles show fitness differences in one environment, but not in a contrasting environment. Ecological genetics in natural populations of perennial or outcrossing plants can also differ substantially from model systems. In this review of the evolutionary genetics of plant adaptation, we emphasize the importance of field studies for understanding the evolutionary dynamics of model and nonmodel systems, highlight a key life history trait (flowering time) and discuss emerging conservation issues.     

High rate of adaptive evolution in two widespread European pines

Comparing related organisms with differing ecological requirements and evolutionary histories can shed light on the mechanisms and drivers underlying genetic adaptation. Here, by examining a common set of hundreds of loci, we compare patterns of nucleotide diversity and molecular adaptation of two European conifers (Scots pine and maritime pine) living in contrasted environments and characterized by distinct population genetic structure (low and clinal in Scots pine, high and ecotypic in maritime pine) and demographic histories. We found higher nucleotide diversity in Scots pine than in maritime pine, whereas rates of new adaptive substitutions (ω_a), as estimated from the distribution of fitness effects, were similar across species and among the highest found in plants. Sample size and population genetic structure did not appear to have resulted in significant bias in estimates of ω_a. Moreover, population contraction–expansion dynamics for each species did not affect differentially the rate of adaptive substitution in these two pines. Several methodological and biological factors may underlie the unusually high rate of adaptive evolution of Scots pine and maritime pine. By providing two new case studies with contrasting evolutionary histories, we contribute to disentangling the multiple factors potentially affecting adaptive evolution in natural plant populations.     

Spatiotemporal landscape genetics: Investigating ecology and evolution through space and time

Genetic time‐series data from historical samples greatly facilitate inference of past population dynamics and species evolution. Yet, although climate and landscape change are often touted as post‐hoc explanations of biological change, our understanding of past climate and landscape change influences on evolutionary processes is severely hindered by the limited application of methods that directly relate environmental change to species dynamics through time. Increased integration of spatiotemporal environmental and genetic data will revolutionize the interpretation of environmental influences on past population processes and the quantification of recent anthropogenic impacts on species, and vastly improve prediction of species responses under future climate change scenarios, yielding widespread revelations across evolutionary biology, landscape ecology and conservation genetics. This review encourages greater use of spatiotemporal landscape genetic analyses that explicitly link landscape, climate and genetic data through time by providing an overview of analytical approaches for integrating historical genetic and environmental data in five key research areas: population genetic structure, demography, phylogeography, metapopulation connectivity and adaptation. We also include a tabular summary of key methodological information, suggest approaches for mitigating the particular difficulties in applying these techniques to ancient DNA and palaeoclimate data, and highlight areas for future methodological development.     

Population genetics and the evolution of geographic range limits in an annual plant

Abstract Theoretical models of species' geographic range limits have identified both demographic and evolutionary mechanisms that prevent range expansion. Stable range limits have been paradoxical for evolutionary biologists because they represent locations where populations chronically fail to respond to selection. Distinguishing among the proposed causes of species' range limits requires insight into both current and historical population dynamics. The tools of molecular population genetics provide a window into the stability of range limits, historical demography, and rates of gene flow. Here we evaluate alternative range limit models using a multilocus data set based on DNA sequences and microsatellites along with field demographic data from the annual plant Clarkia xantiana ssp. xantiana. Our data suggest that central and peripheral populations have very large historical and current effective population sizes and that there is little evidence for population size changes or bottlenecks associated with colonization in peripheral populations. Whereas range limit populations appear to have been stable, central populations exhibit a signature of population expansion and have contributed asymmetrically to the genetic diversity of peripheral populations via migration. Overall, our results discount strictly demographic models of range limits and more strongly support evolutionary genetic models of range limits, where adaptation is prevented by a lack of genetic variation or maladaptive gene flow.     

The evolution of plasticity at geographic range edges

Phenotypic plasticity enables rapid responses to environmental change, and could facilitate range shifts in response to climate change. What drives the evolution of plasticity at range edges, and the capacity of range-edge individuals to be plastic, remain unclear. Here, we propose that accurately predicting when plasticity itself evolves or mediates adaptive evolution at expanding range edges requires integrating knowledge on the demography and evolution of edge populations. Our synthesis shows that: (i) the demography of edge populations can amplify or attenuate responses to selection for plasticity through diverse pathways, and (ii) demographic effects on plasticity are modified by the stability of range edges. Our spatially explicit synthesis for plasticity has the potential to improve predictions for range shifts with climate change.     

Evolutionary rescue in vertebrates: evidence,applications and uncertainty

The current rapid rate of human-driven environmental change presents wild populations with novel conditions and stresses. Theory and experimental evidence for evolutionary rescue present a promising case for species facing environmental change persisting via adaptation. Here, we assess the potential for evolutionary rescue in wild vertebrates. Available information on evolutionary rescue was rare and restricted to abundant and highly fecund species that faced severe intentional anthropogenic selective pressures. However, examples from adaptive tracking in common species and genetic rescues in species of conservation concern provide convincing evidence in favour of the mechanisms of evolutionary rescue. We conclude that low population size, long generation times and limited genetic variability will result in evolutionary rescue occurring rarely for endangered species without intervention. Owing to the risks presented by current environmental change and the possibility of evolutionary rescue in nature, we suggest means to study evolutionary rescue by mapping genotype → phenotype → demography → fitness relationships, and priorities for applying evolutionary rescue to wild populations.     

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

Novel environmental conditions experienced by introduced species can drive rapid evolution of diverse traits. In turn, rapid evolution, both adaptive and non‐adaptive, can influence population size, growth rate, and other important ecological characteristics of populations. In addition, spatial evolutionary processes that arise from a combination of assortative mating between highly dispersive individuals at the expanding edge of populations and altered reproductive rates of those individuals can accelerate expansion speed. Growing experimental evidence shows that the effects of rapid evolution on ecological dynamics can be quite large, and thus it can affect establishment, persistence, and the distribution of populations. We review the experimental and theoretical literature on such eco‐evolutionary feedbacks and evaluate the implications of these processes for biological control. Experiments show that evolving populations can establish at higher rates and grow larger than non‐evolving populations. However, non‐adaptive processes, such as genetic drift and inbreeding depression can also lead to reduced fitness and declines in population size. Spatial evolutionary processes can increase spread rates and change the fitness of individuals at the expansion front. These examples demonstrate the power of eco‐evolutionary dynamics and indicate that evolution is likely more important in biocontrol programs than previously realized. We discuss how this knowledge can be used to enhance efficacy of biological control.     

Running to stand still: adaptation and the response of plants to rapid climate change

Climate is a potent selective force in natural populations, yet the importance of adaptation in the response of plant species to past climate change has been questioned. As many species are unlikely to migrate fast enough to track the rapidly changing climate of the future, adaptation must play an increasingly important role in their response. In this paper we review recent work that has documented climate‐related genetic diversity within populations or on the microgeographical scale. We then describe studies that have looked at the potential evolutionary responses of plant populations to future climate change. We argue that in fragmented landscapes, rapid climate change has the potential to overwhelm the capacity for adaptation in many plant populations and dramatically alter their genetic composition. The consequences are likely to include unpredictable changes in the presence and abundance of species within communities and a reduction in their ability to resist and recover from further environmental perturbations, such as pest and disease outbreaks and extreme climatic events. Overall, a range‐wide increase in extinction risk is likely to result. We call for further research into understanding the causes and consequences of the maintenance and loss of climate‐related genetic diversity within populations.     

Time to Evolve? Potential Evolutionary Responses of Fraser River Sockeye Salmon to Climate Change and Effects on Persistence

Evolutionary adaptation affects demographic resilience to climate change but few studies have attempted to project changes in selective pressures or quantify impacts of trait responses on population dynamics and extinction risk. We used a novel individual-based model to explore potential evolutionary changes in migration timing and the consequences for population persistence in sockeye salmon Oncorhynchus nerka in the Fraser River, Canada, under scenarios of future climate warming. Adult sockeye salmon are highly sensitive to increases in water temperature during their arduous upriver migration, raising concerns about the fate of these ecologically, culturally, and commercially important fish in a warmer future. Our results suggest that evolution of upriver migration timing could allow these salmon to avoid increasingly frequent stressful temperatures, with the odds of population persistence increasing in proportion to the trait heritability and phenotypic variance. With a simulated 2°C increase in average summer river temperatures by 2100, adult migration timing from the ocean to the river advanced by ～10 days when the heritability was 0.5, while the risk of quasi-extinction was only 17% of that faced by populations with zero evolutionary potential (i.e., heritability fixed at zero). The rates of evolution required to maintain persistence under simulated scenarios of moderate to rapid warming are plausible based on estimated heritabilities and rates of microevolution of timing traits in salmon and related species, although further empirical work is required to assess potential genetic and ecophysiological constraints on phenological adaptation. These results highlight the benefits to salmon management of maintaining evolutionary potential within populations, in addition to conserving key habitats and minimizing additional stressors where possible, as a means to build resilience to ongoing climate change. More generally, they demonstrate the importance and feasibility of considering evolutionary processes, in addition to ecology and demography, when projecting population responses to environmental change.     

Population differentiation in the context of Holocene climate change for a migratory marine species,the southern elephant seal

Understanding observed patterns of connectivity requires an understanding of the evolutionary processes that determine genetic structure among populations, with the most common models being associated with isolation by distance, allopatry or vicariance. Pinnipeds are annual breeders with the capacity for extensive range overlap during seasonal migrations, establishing the potential for the evolution of isolation by distance. Here, we assess the pattern of differentiation among six breeding colonies of the southern elephant seal, Mirounga leonina, based on mtDNA and 15 neutral microsatellite DNA markers, and consider measures of their demography and connectivity. We show that all breeding colonies are genetically divergent and that connectivity in this highly mobile pinniped is not strongly associated with geographic distance, but more likely linked to Holocene climate change and demographic processes. Estimates of divergence times between populations were all after the last glacial maximum, and there was evidence for directional migration in a clockwise pattern (with the prevailing current) around the Antarctic. We discuss the mechanisms by which climate change may have contributed to the contemporary genetic structure of southern elephant seal populations and the broader implications.     

Landscape genetics of plants

Landscape genetics is the amalgamation of landscape ecology and population genetics to help with understanding microevolutionary processes such as gene flow and adaptation. In this review, we examine why landscape genetics of plants lags behind that of animals, both in number of studies and consideration of landscape elements. The classical landscape distance/resistance approach to study gene flow is challenging in plants, whereas boundary detection and the assessment of contemporary gene flow are more feasible. By contrast, the new field of landscape genetics of adaptive genetic variation, establishing the relationship between adaptive genomic regions and environmental factors in natural populations, is prominent in plant studies. Landscape genetics is ideally suited to study processes such as migration and adaptation under global change.     

EXPERIMENTAL EVOLUTION MEETS MARINE PHYTOPLANKTON

Our perspective highlights potentially important links between disparate fields—biological oceanography, climate change research, and experimental evolutionary biology. We focus on one important functional group—photoautotrophic microbes (phytoplankton), which are responsible for ～50% of global primary productivity. Global climate change currently results in the simultaneous change of several conditions such as warming, acidification, and nutrient supply. It thus has the potential to dramatically change phytoplankton physiology, community composition, and may result in adaptive evolution. Although their large population sizes, standing genetic variation, and rapid turnover time should promote swift evolutionary change, oceanographers have focussed on describing patterns of present day physiological differentiation rather than measure potential adaptation in evolution experiments, the only direct way to address whether and at which rate phytoplankton species will adapt to environmental change. Important open questions are (1) is adaptation limited by existing genetic variation or fundamental constraints? (2) Will complex ecological settings such as gradual versus abrupt environmental change influence adaptation processes? (3) How will increasing environmental variability affect the evolution of phenotypic plasticity patterns? Because marine phytoplankton species display rapid acclimation capacity (phenotypic buffering), a systematic study of reaction norms renders them particularly interesting to the evolutionary biology research community.     

Rate of adaptive peak shifts with partial genetic robustness

How adaptive evolution occurs with individually deleterious but jointly beneficial mutations has been one of the major problems in population genetics theory. Adaptation in this case is commonly described as a population's escape from a local peak to a higher peak on Sewall Wright's fitness landscape. Recent molecular genetic and computational studies have suggested that genetic robustness can facilitate such peak shifts. If phenotypic expressions of new mutations are suppressed under genetic robustness, mutations that are otherwise deleterious can accumulate in the population as neutral variants. When the robustness is perturbed by an environmental change or a major mutation, these variants become exposed to natural selection. It is argued that this process promotes adaptation because allelic combinations enriched under genetic robustness can then be positively selected. Here, I propose simple two- and three-locus models of adaptation with partial genetic robustness as suggested by recent studies. The waiting time until the fixation of an adaptive haplotype was observed in stochastic simulations and compared to the expectation without robustness. It is shown that peak shifts can be delayed or accelerated depending on the conditions of genetic robustness. The evolutionary significance of these processes is discussed.     

The long and winding road of evolutionary demography: preface

Fitness can be calculated using demographic parameters such as survival and fecundity, which are normally used to examine population dynamics in ecology. This concept is at the heart of Darwin's thinking on natural selection. Natural selection optimizes survival and fertility schedules through differential fitness, and these optimal schedules drive changes in population dynamics. Therefore, there must exist an interaction between ecology and evolution. One of the disciplines that focus on the interaction is "Evolutionary demography". It uses age- or stage-specific demographic parameters throughout the whole life history to explore the evolution of life histories. Data throughout the life history of a species is indispensable to study evolutionary demography. To this end, two large-scale databases of plant and animal life history are now available online, the COMPADRE Plant Matrix Database and the COMADRE Animal Matrix Database. We are now in a revolutionary era in the demographic research of plant and animal populations (including human populations). Many skills and approaches are needed to answer questions on evolutionary demography including bodies of theory and analytical toolkits. This special issue covers a wide array of subjects: (1) Demographic analysis of populations (including human populations) from the point of view of evolutionary ecology, (2) Meta-analysis using big databases of populations, (3) Eco-evolutionary studies at the population and/or community level and (4) Theoretical studies and the development of mathematical models of life history evolution. 14 collected papers are published to answer a variety of questions using original ideas, new tools, and big data.     

Rapid,nonparallel genomic evolution of Brassica rapa (field mustard) under experimental drought

While we know that climate change can potentially cause rapid phenotypic evolution, our understanding of the genetic basis and degree of genetic parallelism of rapid evolutionary responses to climate change is limited. In this study, we combined the resurrection approach with an evolve-and-resequence design to examine genome-wide evolutionary changes following drought. We exposed genetically similar replicate populations of the annual plant Brassica rapa derived from a field population in southern California to four generations of experimental drought or watered conditions in a greenhouse. Genome-wide sequencing of ancestral and descendant population pools identified hundreds of SNPs that showed evidence of rapidly evolving in response to drought. Several of these were in stress response genes, and two were identified in a prior study of drought response in this species. However, almost all genetic changes were unique among experimental populations, indicating that the evolutionary changes were largely nonparallel, despite the fact that genetically similar replicates of the same founder population had experienced controlled and consistent selection regimes. This nonparallelism of evolution at the genetic level is potentially because of polygenetic adaptation allowing for multiple different genetic routes to similar phenotypic outcomes. Our findings help to elucidate the relationship between rapid phenotypic and genomic evolution and shed light on the degree of parallelism and predictability of genomic evolution to environmental change.