Evolutionary rescue and adaptation to abrupt environmental change depends upon the history of stress

Whether evolution will be rapid enough to rescue declining populations will depend upon population size, the supply of genetic variation, the degree of maladaptation and the historical direction of selection. We examined whether the level of environmental stress experienced by a population prior to abrupt environmental change affects the probability of evolutionary rescue (ER). Hundreds of populations of two species of yeast, Saccharomyces cerevisiae and Saccharomyces paradoxus were exposed to a range of sublethal concentrations of salt for approximately a hundred generations before transfer to a concentration of salt lethal to the ancestor (150 g l^–1 NaCl). The fitness of surviving populations of both species was a quadratic function of yield: fitness was greatest for large populations that had been selected on low salt concentrations (less than 20 g l⁻¹ NaCl) and small populations that had adapted to high salt (more than 80 g l⁻¹ NaCl). However, differences occurred between species in the probability of ER. The frequency of ER was positively correlated with salt concentration for S. cerevisiae, but negatively correlated with salt concentration in S. paradoxus. These results not only demonstrate that past environmental conditions can determine the probability of ER after abrupt environmental change, but also suggest that there may even be differences between closely related species that are worth further exploration.     

Evolutionary rescue in randomly mating,selfing, and clonal populations

Severe environmental change can drive a population extinct unless the population adapts in time to the new conditions (“evolutionary rescue”). How does biparental sexual reproduction influence the chances of population persistence compared to clonal reproduction or selfing? In this article, we set up a one‐locus two‐allele model for adaptation in diploid species, where rescue is contingent on the establishment of the mutant homozygote. Reproduction can occur by random mating, selfing, or clonally. Random mating generates and destroys the rescue mutant; selfing is efficient at generating it but at the same time depletes the heterozygote, which can lead to a low mutant frequency in the standing genetic variation. Due to these (and other) antagonistic effects, we find a nontrivial dependence of population survival on the rate of sex/selfing, which is strongly influenced by the dominance coefficient of the mutation before and after the environmental change. Importantly, since mating with the wild‐type breaks the mutant homozygote up, a slow decay of the wild‐type population size can impede rescue in randomly mating populations.     

EVOLUTIONARY RESCUE OF SEXUAL AND ASEXUAL POPULATIONS IN A DETERIORATING ENVIRONMENT

The environmental change experienced by many contemporary populations of organisms poses a serious risk to their survival. From the theory of evolutionary rescue, we predict that the combination of sex and genetic diversity should increase the probability of survival by increasing variation and thereby the probability of generating a type that can tolerate the stressful environment. We tested this prediction by comparing experimental populations of Chlamydomonas reinhardtii that differ in sexuality and in the initial amount of genetic diversity. The lines were serially propagated in an environment where the level of stress caused by salt increased over time from fresh water to the limits of marine conditions. In the long term, the combination of high diversity and obligate sexuality was most effective in supporting evolutionary rescue. Most of the adaptation to high‐salt environments in the obligate sexual‐high diversity lines had occurred by midway through the experiment, indicating that positive genetic correlations of adaptation to lethal stress with adaptation to sublethal stress greatly increased the probability of evolutionary rescue. The evolutionary rescue events observed in this study provide evidence that major shifts in ways of life can arise within short time frames through the action of natural selection in sexual populations.     

What invasive species reveal about the rate and form of contemporary phenotypic change in nature

Biological invasions are opportunities to gain insight into fundamental evolutionary questions, because reproductive isolation and sudden alterations in selection pressures are likely to lead to rapid evolutionary change. Here I investigate the role played by invasive species in revealing the rate and form of contemporary phenotypic change in wild populations by expanding a database of more than 5,500 rates of phenotypic change from 90 species of plants and animals. Invasive species are frequently used as model organisms and thus contribute disproportionately to available rates of phenotypic change. However, the preponderance of these rates is the consequence of extensive study in a small number of species. I found mixed evidence to support the hypothesis that phenotypic change is associated with time depending on the metric of choice (i.e., darwins or haldanes). Insights from both invasive and native species provide evidence for abrupt phenotypic change and suggest that the environment plays a potentially important role in driving trait change in wild populations, although the environmental influence on the observed trajectories remains unclear. Thus, future work should continue to seek an understanding of the mechanistic underpinnings--both genetic and environmental--of how phenotypic variation allows populations to adapt to rapidly changing global environments.     

Centennial clonal stability of asexual Daphnia in Greenland lakes despite climate variability

Climate and environmental condition drive biodiversity at many levels of biological organization, from populations to ecosystems. Combined with paleoecological reconstructions, palaeogenetic information on resident populations provides novel insights into evolutionary trajectories and genetic diversity driven by environmental variability. While temporal observations of changing genetic structure are often made of sexual populations, little is known about how environmental change affects the long‐term fate of asexual lineages. Here, we provide information on obligately asexual, triploid Daphnia populations from three Arctic lakes in West Greenland through the past 200–300 years to test the impact of environmental change on the temporal and spatial population genetic structure. The contrasting ecological state of the lakes, specifically regarding salinity and habitat structure may explain the observed lake‐specific clonal composition over time. Palaeolimnological reconstructions show considerable regional environmental fluctuations since 1,700 (the end of the Little Ice Age), but the population genetic structure in two lakes was almost unchanged with at most two clones per time period. Their local populations were strongly dominated by a single clone that has persisted for 250–300 years. We discuss possible explanations for the apparent population genetic stability: (a) persistent clones are general‐purpose genotypes that thrive under broad environmental conditions, (b) clonal lineages evolved subtle genotypic differences unresolved by microsatellite markers, or (c) epigenetic modifications allow for clonal adaptation to changing environmental conditions. Our results motivate research into the mechanisms of adaptation in these populations, as well as their evolutionary fate in the light of accelerating climate change in the polar regions.     

Avoiding extinction under nonlinear environmental change: models of evolutionary rescue with plasticity

Rapid environmental changes are putting numerous species at risk of extinction. For migration-limited species, persistence depends on either phenotypic plasticity or evolutionary adaptation (evolutionary rescue). Current theory on evolutionary rescue typically assumes linear environmental change. Yet accelerating environmental change may pose a bigger threat. Here, we present a model of a species encountering an environment with accelerating or decelerating change, to which it can adapt through evolution or phenotypic plasticity (within-generational or transgenerational). We show that unless either form of plasticity is sufficiently strong or adaptive genetic variation is sufficiently plentiful, accelerating or decelerating environmental change increases extinction risk compared to linear environmental change for the same mean rate of environmental change.     

The role of anthropogenic dispersal in shaping the distribution and genetic composition of a widespread North American tree species

Dispersal and colonization are among the most important ecological processes for species persistence as they allow species to track changing environmental conditions. During the last glacial maximum (LGM), many cold‐intolerant Northern Hemisphere plants retreated to southern glacial refugia. During subsequent warming periods, these species expanded their ranges northward. Interestingly, some tree species with limited seed dispersal migrated considerable distances after the LGM ~19,000 years before present (YBP). It has been hypothesized that indigenous peoples may have dispersed valued species, in some cases beyond the southern limits of the Laurentide Ice Sheet. To investigate this question, we employed a molecular genetics approach on a widespread North American understory tree species whose fruit was valued by indigenous peoples. Twenty putative anthropogenic (near pre‐Columbian habitations) and 62 wild populations of Asimina triloba (pawpaw), which produces the largest edible fruit of any North American tree, were genetically assayed with nine microsatellite loci. Putative anthropogenic populations were characterized by reduced genetic diversity and greater excess heterozygosity relative to wild populations. Anthropogenic populations in regions that were glaciated during the LGM had profiles consistent with founder effects and reduced gene flow, and shared rare alleles with wild populations hundreds of kilometers away (mean = 723 km). Some of the most compelling evidence for human‐mediated dispersal is that putative anthropogenic and wild populations sharing rare alleles were separated by significantly greater distances (mean = 695 km) than wild populations sharing rare alleles (mean = 607 km; p = .014). Collectively, the genetic data suggest that long‐distance dispersal played an important role in the distribution of pawpaw and is consistent with the hypothesized role of indigenous peoples.     

Genetic conservation and management of the California endemic,Torrey pine (Pinus torreyana Parry): Implications of genetic rescue in a genetically depauperate species

Rare species present a challenge under changing environmental conditions as the genetic consequences of rarity may limit species ability to adapt to environmental change. To evaluate the evolutionary potential of a rare species, we assessed variation in traits important to plant fitness using multigenerational common garden experiments. Torrey pine, Pinus torreyana Parry, is one of the rarest pines in the world, restricted to one mainland and one island population. Morphological differentiation between island and mainland populations suggests adaptation to local environments may have contributed to trait variation. The distribution of phenotypic variances within the common garden suggests distinct population‐specific growth trajectories underlay genetic differences, with the island population exhibiting substantially reduced genetic variance for growth relative to the mainland population. Furthermore, F1 hybrids, representing a cross between mainland and island trees, exhibit increased height accumulation and fecundity relative to mainland and island parents. This may indicate genetic rescue via intraspecific hybridization could provide the necessary genetic variation to persist in environments modified as a result of climate change. Long‐term common garden experiments, such as these, provide invaluable resources to assess the distribution of genetic variance that may inform conservation strategies to preserve evolutionary potential of rare species, including genetic rescue.     

Evolutionary constraints mediate extinction risk under climate change

Mounting evidence suggests that rapid evolutionary adaptation may rescue some organisms from the impacts of climate change. However, evolutionary constraints might hinder this process, especially when different aspects of environmental change generate antagonistic selection on genetically correlated traits. Here, we use individual-based simulations to explore how genetic correlations underlying the thermal physiology of ectotherms might influence their responses to the two major components of climate change—increases in mean temperature and thermal variability. We found that genetic correlations can influence population dynamics under climate change, with declines in population size varying three-fold depending on the type of correlation present. Surprisingly, populations whose thermal performance curves were constrained by genetic correlations often declined less rapidly than unconstrained populations. Our results suggest that accurate forecasts of the impact of climate change on ectotherms will require an understanding of the genetic architecture of the traits under selection.     

IBSEM: An Individual-Based Atlantic Salmon Population Model

Ecology and genetics can influence the fate of individuals and populations in multiple ways. However, to date, few studies consider them when modelling the evolutionary trajectory of populations faced with admixture with non-local populations. For the Atlantic salmon, a model incorporating these elements is urgently needed because many populations are challenged with gene-flow from non-local and domesticated conspecifics. We developed an Individual-Based Salmon Eco-genetic Model (IBSEM) to simulate the demographic and population genetic change of an Atlantic salmon population through its entire life-cycle. Processes such as growth, mortality, and maturation are simulated through stochastic procedures, which take into account environmental variables as well as the genotype of the individuals. IBSEM is based upon detailed empirical data from salmon biology, and parameterized to reproduce the environmental conditions and the characteristics of a wild population inhabiting a Norwegian river. Simulations demonstrated that the model consistently and reliably reproduces the characteristics of the population. Moreover, in absence of farmed escapees, the modelled populations reach an evolutionary equilibrium that is similar to our definition of a ‘wild’ genotype. We assessed the sensitivity of the model in the face of assumptions made on the fitness differences between farm and wild salmon, and evaluated the role of straying as a buffering mechanism against the intrusion of farm genes into wild populations. These results demonstrate that IBSEM is able to capture the evolutionary forces shaping the life history of wild salmon and is therefore able to model the response of populations under environmental and genetic stressors.     

Environmental quality and evolutionary potential: lessons from wild populations

An essential requirement to determine a population's potential for evolutionary change is to quantify the amount of genetic variability expressed for traits under selection. Early investigations in laboratory conditions showed that the magnitude of the genetic and environmental components of phenotypic variation can change with environmental conditions. However, there is no consensus as to how the expression of genetic variation is sensitive to different environmental conditions. Recently, the study of quantitative genetics in the wild has been revitalized by new pedigree analyses based on restricted maximum likelihood, resulting in a number of studies investigating these questions in wild populations. Experimental manipulation of environmental quality in the wild, as well as the use of naturally occurring favourable or stressful environments, has broadened the treatment of different taxa and traits. Here, we conduct a meta-analysis on recent studies comparing heritability in favourable versus unfavourable conditions in non-domestic and non-laboratory animals. The results provide evidence for increased heritability in more favourable conditions, significantly so for morphometric traits but not for traits more closely related to fitness. We discuss how these results are explained by underlying changes in variance components, and how they represent a major step in our understanding of evolutionary processes in wild populations. We also show how these trends contrast with the prevailing view resulting mainly from laboratory experiments on Drosophila. Finally, we underline the importance of taking into account the environmental variation in models predicting quantitative trait evolution.     

Relationships between population density,fine-scale genetic structure,mating system and pollen dispersal in a timber tree from African rainforests

Owing to the reduction of population density and/or the environmental changes it induces, selective logging could affect the demography, reproductive biology and evolutionary potential of forest trees. This is particularly relevant in tropical forests where natural population densities can be low and isolated trees may be subject to outcross pollen limitation and/or produce low-quality selfed seeds that exhibit inbreeding depression. Comparing reproductive biology processes and genetic diversity of populations at different densities can provide indirect evidence of the potential impacts of logging. Here, we analysed patterns of genetic diversity, mating system and gene flow in three Central African populations of the self-compatible legume timber species Erythrophleum suaveolens with contrasting densities (0.11, 0.68 and 1.72 adults per ha). The comparison of inbreeding levels among cohorts suggests that selfing is detrimental as inbred individuals are eliminated between seedling and adult stages. Levels of genetic diversity, selfing rates (∼16%) and patterns of spatial genetic structure (Sp ∼0.006) were similar in all three populations. However, the extent of gene dispersal differed markedly among populations: the average distance of pollen dispersal increased with decreasing density (from 200 m in the high-density population to 1000 m in the low-density one). Overall, our results suggest that the reproductive biology and genetic diversity of the species are not affected by current logging practices. However, further investigations need to be conducted in low-density populations to evaluate (1) whether pollen limitation may reduce seed production and (2) the regeneration potential of the species.     

Temporal genetic stability in natural populations of the waterflea Daphnia magna in response to strong selection pressure

Studies monitoring changes in genetic diversity and composition through time allow a unique understanding of evolutionary dynamics and persistence of natural populations. However, such studies are often limited to species with short generation times that can be propagated in the laboratory or few exceptional cases in the wild. Species that produce dormant stages provide powerful models for the reconstruction of evolutionary dynamics in the natural environment. A remaining open question is to what extent dormant egg banks are an unbiased representation of populations and hence of the species’ evolutionary potential, especially in the presence of strong environmental selection. We address this key question using the water flea Daphnia magna, which produces dormant stages that accumulate in biological archives over time. We assess temporal genetic stability in three biological archives, previously used in resurrection ecology studies showing adaptive evolutionary responses to rapid environmental change. We show that neutral genetic diversity does not decline with the age of the population and it is maintained in the presence of strong selection. In addition, by comparing temporal genetic stability in hatched and unhatched populations from the same biological archive, we show that dormant egg banks can be consulted to obtain a reliable measure of genetic diversity over time, at least in the multidecadal time frame studied here. The stability of neutral genetic diversity through time is likely mediated by the buffering effect of the resting egg bank.     

Environmental Variables Explain Genetic Structure in a Beetle-Associated Nematode

The distribution of a species is a complex expression of its ecological and evolutionary history and integrating population genetic, environmental, and ecological data can provide new insights into the effects of the environment on the population structure of species. Previous work demonstrated strong patterns of genetic differentiation in natural populations of the hermaphroditic nematode Pristionchus pacificus in its La Réunion Island habitat, but gave no clear understanding of the role of the environment in structuring this variation. Here, we present what is to our knowledge the first study to statistically evaluate the role of the environment in shaping the structure and distribution of nematode populations. We test the hypothesis that genetic structure in P. pacificus is influenced by environmental variables, by combining population genetic analyses of microsatellite data from 18 populations and 370 strains, with multivariate statistics on environmental data, and species distribution modelling. We assess and quantify the relative importance of environmental factors (geographic distance, altitude, temperature, precipitation, and beetle host) on genetic variation among populations. Despite the fact that geographic populations of P. pacificus comprise vast genetic diversity sourced from multiple ancestral lineages, we find strong evidence for local associations between environment and genetic variation. Further, we show that significantly more genetic variation in P. pacificus populations is explained by environmental variation than by geographic distances. This supports a strong role for environmental heterogeneity vs. genetic drift in the divergence of populations, which we suggest may be influenced by adaptive forces.     

Thermal tolerance in the keystone species Daphnia magna—a candidate gene and an outlier analysis approach

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long‐term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm‐ and cold‐adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST‐linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.     

Land use causes genetic differentiation of life‐history traits in Bromus hordeaceus

There is increasing evidence that species can evolve rapidly in response to environmental change. However, although land use is one of the key drivers of current environmental change, studies of its evolutionary consequences are still fairly scarce, in particular studies that examine land‐use effects across large numbers of populations, and discriminate between different aspects of land use. Here, we investigated genetic differentiation in relation to land use in the annual grass Bromus hordeaceus. A common garden study with offspring from 51 populations from three regions and a broad range of land‐use types and intensities showed that there was indeed systematic population differentiation of ecologically important plant traits in relation to land use, in particular due to increasing mowing and grazing intensities. We also found strong land‐use‐related genetic differentiation in plant phenology, where the onset of flowering consistently shifted away from the typical time of management. In addition, increased grazing intensity significantly increased the genetic variability within populations. Our study suggests that land use can cause considerable genetic differentiation among plant populations, and that the timing of land use may select for phenological escape strategies, particularly in monocarpic plant species.     

Rapid Parallel Adaptation to Anthropogenic Heavy Metal Pollution

The impact of human-mediated environmental change on the evolutionary trajectories of wild organisms is poorly understood. In particular, capacity of species to adapt rapidly (in hundreds of generations or less), reproducibly and predictably to extreme environmental change is unclear. Silene uniflora is predominantly a coastal species, but it has also colonized isolated, disused mines with phytotoxic, zinc-contaminated soils. To test whether rapid, parallel adaptation to anthropogenic pollution has taken place, we used reduced representation sequencing (ddRAD) to reconstruct the evolutionary history of geographically proximate mine and coastal population pairs and found largely independent colonization of mines from different coastal sites. Furthermore, our results show that parallel evolution of zinc tolerance has occurred without gene flow spreading adaptive alleles between mine populations. In genomic regions where signatures of selection were detected across multiple mine-coast pairs, we identified genes with functions linked to physiological differences between the putative ecotypes, although genetic differentiation at specific loci is only partially shared between mine populations. Our results are consistent with a complex, polygenic genetic architecture underpinning rapid adaptation. This shows that even under a scenario of strong selection and rapid adaptation, evolutionary responses to human activities (and other environmental challenges) may be idiosyncratic at the genetic level and, therefore, difficult to predict from genomic data.     

Eco‐evolutionary dynamics in response to selection on life‐history

Understanding the consequences of environmental change on ecological and evolutionary dynamics is inherently problematic because of the complex interplay between them. Using invertebrates in microcosms, we characterise phenotypic, population and evolutionary dynamics before, during and after exposure to a novel environment and harvesting over 20 generations. We demonstrate an evolved change in life‐history traits (the age‐ and size‐at‐maturity, and survival to maturity) in response to selection caused by environmental change (wild to laboratory) and to harvesting (juvenile or adult). Life‐history evolution, which drives changes in population growth rate and thus population dynamics, includes an increase in age‐to‐maturity of 76% (from 12.5 to 22 days) in the unharvested populations as they adapt to the new environment. Evolutionary responses to harvesting are outweighed by the response to environmental change (~ 1.4 vs. 4% change in age‐at‐maturity per generation). The adaptive response to environmental change converts a negative population growth trajectory into a positive one: an example of evolutionary rescue.     

Moving beyond heritability in the search for coral adaptive potential

Global environmental change is happening at unprecedented rates. Coral reefs are among the ecosystems most threatened by global change. For wild populations to persist, they must adapt. Knowledge shortfalls about corals' complex ecological and evolutionary dynamics, however, stymie predictions about potential adaptation to future conditions. Here, we review adaptation through the lens of quantitative genetics. We argue that coral adaptation studies can benefit greatly from “wild” quantitative genetic methods, where traits are studied in wild populations undergoing natural selection, genomic relationship matrices can replace breeding experiments, and analyses can be extended to examine genetic constraints among traits. In addition, individuals with advantageous genotypes for anticipated future conditions can be identified. Finally, genomic genotyping supports simultaneous consideration of how genetic diversity is arrayed across geographic and environmental distances, providing greater context for predictions of phenotypic evolution at a metapopulation scale.