From nature to the laboratory: the impact of founder effects on adaptation

Most founding events entail a reduction in population size, which in turn leads to genetic drift effects that can deplete alleles. Besides reducing neutral genetic variability, founder effects can in principle shift additive genetic variance for phenotypes that underlie fitness. This could then lead to different rates of adaptation among populations that have undergone a population size bottleneck as well as an environmental change, even when these populations have a common evolutionary history. Thus, theory suggests that there should be an association between observable genetic variability for both neutral markers and phenotypes related to fitness. Here, we test this scenario by monitoring the early evolutionary dynamics of six laboratory foundations derived from founders taken from the same source natural population of Drosophila subobscura. Each foundation was in turn three‐fold replicated. During their first few generations, these six foundations showed an abrupt increase in their genetic differentiation, within and between foundations. The eighteen populations that were monitored also differed in their patterns of phenotypic adaptation according to their immediately ancestral founding sample. Differences in early genetic variability and in effective population size were found to predict differences in the rate of adaptation during the first 21 generations of laboratory evolution. We show that evolution in a novel environment is strongly contingent not only on the initial composition of a newly founded population but also on the stochastic changes that occur during the first generations of colonization. Such effects make laboratory populations poor guides to the evolutionary genetic properties of their ancestral wild populations.     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Rapid divergence and convergence of life‐history in experimentally evolved Drosophila melanogaster

Laboratory selection experiments are alluring in their simplicity, power, and ability to inform us about how evolution works. A longstanding challenge facing evolution experiments with metazoans is that significant generational turnover takes a long time. In this work, we present data from a unique system of experimentally evolved laboratory populations of Drosophila melanogaster that have experienced three distinct life‐history selection regimes. The goal of our study was to determine how quickly populations of a certain selection regime diverge phenotypically from their ancestors, and how quickly they converge with independently derived populations that share a selection regime. Our results indicate that phenotypic divergence from an ancestral population occurs rapidly, within dozens of generations, regardless of that population's evolutionary history. Similarly, populations sharing a selection treatment converge on common phenotypes in this same time frame, regardless of selection pressures those populations may have experienced in the past. These patterns of convergence and divergence emerged much faster than expected, suggesting that intermediate evolutionary history has transient effects in this system. The results we draw from this system are applicable to other experimental evolution projects, and suggest that many relevant questions can be sufficiently tested on shorter timescales than previously thought.     

Evolutionary adaptation to freeze-thaw-growth cycles in Escherichia coli

Fifteen populations of Escherichia coli were propagated for 150 freeze-thaw-growth (FTG) cycles in order to study the phenotypic and genetic changes that evolve under these stressful conditions. Here we present the phenotypic differences between the evolved lines and their progenitors as measured by competition experiments and growth curves. Three FTG lines evolved from an ancestral strain that was previously used to start a long-term evolution experiment, while the other 12 FTG lines are derived from clones that had previously evolved for 20,000 generations at constant 37 degrees C. Competition experiments indicate that the former FTG group improved their mean fitness under the FTG regime by about 90% relative to their progenitor, while the latter FTG group gained on average about 60% relative to their own progenitors. These increases in fitness result from both improved survival during freezing and thawing and more rapid recovery to initiate exponential growth after thawing. This shorter lag phase is specific to recovery after freezing and thawing. Future work will seek to identify the mutations responsible for evolutionary adaptation to the FTG environment and use them to explore the physiological mechanisms that allow increased survival and more rapid recovery.     

Environmental change, phenotypic plasticity, and genetic compensation

When a species encounters novel environmental conditions, some phenotypic characters may develop differently than in the ancestral environment. Most environmental perturbations of development are likely to reduce fitness, and thus selection would usually be expected to favor genetic changes that restore the ancestral phenotype. I propose the term "genetic compensation" to refer to this form of adaptive evolution. Genetic compensation is a subset of genetic accommodation and the reverse of genetic assimilation. When genetic compensation has occurred along a spatial environmental gradient, the mean trait values of populations in different environments may be more similar in the field than when representatives of the same populations are raised in a common environment (i.e., countergradient variation). If compensation is complete, genetic divergence between populations may be cryptic, that is, not detectable in the field. Here I apply the concept of genetic compensation to three examples involving carotenoid-based sexual coloration and then use these and other examples to discuss the concept in a broader context. I show that genetic compensation may lead to a cryptic form of reproductive isolation between populations evolving in different environments, may explain some puzzling cases in which heritable traits exposed to strong directional selection fail to show the expected evolutionary response, and may complicate efforts to monitor populations for signs of environmental deterioration.     

Fitness recovery and compensatory evolution in natural mutant lines of C. elegans

Deleterious mutation accumulation plays a central role in evolutionary genetics, conservation biology, human health, and evolutionary medicine (e.g., methods of viral attenuation for live vaccines). It is therefore important to understand whether and how quickly populations with accumulated deleterious mutational loads can recover fitness through adaptive evolution. We used laboratory experimental evolution with four long-term mutation-accumulation (MA) lines of Caenorhabditis elegans nematodes to study the dynamics of such fitness evolution. We previously showed that when homozygous mutant populations are evolved in large population sizes, they can rapidly achieve wild-type fitness through the accumulation of new beneficial or compensatory epistatic mutations. Here, we expand this approach to demonstrate that when replicate lineages are initiated from the same mutant genotype, phenotypic evolution is only sometimes repeatable. MA genotypes that recovered ancestral fitness in the previous experiment did not always do so here. Further, the pattern of adaptive evolution in independently evolved replicates was contingent upon the MA genotype and varied among fitness-related traits. Our findings suggest that new beneficial mutations can drive rapid fitness evolution, but that the adaptive process is rendered somewhat unpredictable by its susceptibility to chance events and sensitivity to the evolutionary history of the starting population.     

Evolutionary mismatch along salinity gradients in a Neotropical water strider

The evolution of local adaptation is crucial for the in situ persistence of populations in changing environments. However, selection along broad environmental gradients could render local adaptation difficult, and might even result in maladaptation. We address this issue by quantifying fitness trade‐offs (via common garden experiments) along a salinity gradient in two populations of the Neotropical water strider Telmatometra withei—a species found in both fresh (FW) and brackish (BW) water environments across Panama. We found evidence for local adaptation in the FW population in its home FW environment. However, the BW population showed only partial adaptation to the BW environment, with a high magnitude of maladaptation along naturally occurring salinity gradients. Indeed, its overall fitness was ~60% lower than that of the ancestral FW population in its home environment, highlighting the role of phenotypic plasticity, rather than local adaptation, in high salinity environments. This suggests that populations seemingly persisting in high salinity environments might in fact be maladapted, following drastic changes in salinity. Thus, variable selection imposed by salinization could result in evolutionary mismatch, where the fitness of a population is displaced from its optimal environment. Understanding the fitness consequences of persisting in fluctuating salinity environments is crucial to predict the persistence of populations facing increasing salinization. It will also help develop evolutionarily informed management strategies in the context of global change.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.     

Selection analysis on the rapid evolution of a secondary sexual trait

Evolutionary analyses of population translocations (experimental or accidental) have been important in demonstrating speed of evolution because they subject organisms to abrupt environmental changes that create an episode of selection. However, the strength of selection in such studies is rarely measured, limiting our understanding of the evolutionary process. This contrasts with long-term, mark–recapture studies of unmanipulated populations that measure selection directly, yet rarely reveal evolutionary change. Here, we present a study of experimental evolution of male colour in Trinidadian guppies where we tracked both evolutionary change and individual-based measures of selection. Guppies were translocated from a predator-rich to a low-predation environment within the same stream system. We used a combination of common garden experiments and monthly sampling of individuals to measure the phenotypic and genetic divergence of male coloration between ancestral and derived fish. Results show rapid evolutionary increases in orange coloration in both populations (1 year or three generations), replicating the results of previous studies. Unlike previous studies, we linked this evolution to an individual-based analysis of selection. By quantifying individual reproductive success and survival, we show, for the first time, that males with more orange and black pigment have higher reproductive success, but males with more black pigment also have higher risk of mortality. The net effect of selection is thus an advantage of orange but not black coloration, as reflected in the evolutionary response. This highlights the importance of considering all components of fitness when understanding the evolution of sexually selected traits in the wild.     

Phenotypic plasticity in evolutionary rescue experiments

Population persistence in a new and stressful environment can be influenced by the plastic phenotypic responses of individuals to this environment, and by the genetic evolution of plasticity itself. This process has recently been investigated theoretically, but testing the quantitative predictions in the wild is challenging because (i) there are usually not enough population replicates to deal with the stochasticity of the evolutionary process, (ii) environmental conditions are not controlled, and (iii) measuring selection and the inheritance of traits affecting fitness is difficult in natural populations. As an alternative, predictions from theory can be tested in the laboratory with controlled experiments. To illustrate the feasibility of this approach, we briefly review the literature on the experimental evolution of plasticity, and on evolutionary rescue in the laboratory, paying particular attention to differences and similarities between microbes and multicellular eukaryotes. We then highlight a set of questions that could be addressed using this framework, which would enable testing the robustness of theoretical predictions, and provide new insights into areas that have received little theoretical attention to date.     

Adaptive plasticity and niche expansion in an invasive thistle

Phenotypic differentiation in size and fecundity between native and invasive populations of a species has been suggested as a causal driver of invasion in plants. Local adaptation to novel environmental conditions through a micro‐evolutionary response to natural selection may lead to phenotypic differentiation and fitness advantages in the invaded range. Local adaptation may occur along a stress tolerance trade‐off, favoring individuals that, in benign conditions, shift resource allocation from stress tolerance to increased vigor and fecundity and, therefore, invasiveness. Alternately, the typically disturbed invaded range may select for a plastic, generalist strategy, making phenotypic plasticity the main driver of invasion success. To distinguish between these hypotheses, we performed a field common garden and tested for genetically based phenotypic differentiation, resource allocation shifts in response to water limitation, and local adaptation to the environmental gradient which describes the source locations for native and invasive populations of diffuse knapweed (Centaurea diffusa). Plants were grown in an experimental field in France (naturalized range) under water addition and limitation conditions. After accounting for phenotypic variation arising from environmental differences among collection locations, we found evidence of genetic variation between the invasive and native populations for most morphological and life‐history traits under study. Invasive C. diffusa populations produced larger, later maturing, and therefore potentially fitter individuals than native populations. Evidence for local adaptation along a resource allocation trade‐off for water limitation tolerance is equivocal. However, native populations do show evidence of local adaptation to an environmental gradient, a relationship which is typically not observed in the invaded range. Broader analysis of the climatic niche inhabited by the species in both ranges suggests that the physiological tolerances of C. diffusa may have expanded in the invaded range. This observation could be due to selection for plastic, “general‐purpose” genotypes with broad environmental tolerances.     

SLOWLY SWITCHING BETWEEN ENVIRONMENTS FACILITATES REVERSE EVOLUTION IN SMALL POPULATIONS

Natural populations must constantly adapt to ever‐changing environmental conditions. A particularly interesting question is whether such adaptations can be reversed by returning the population to an ancestral environment. Such evolutionary reversals have been observed in both natural and laboratory populations. However, the factors that determine the reversibility of evolution are still under debate. The time scales of environmental change vary over a wide range, but little is known about how the rate of environmental change influences the reversibility of evolution. Here, we demonstrate computationally that slowly switching between environments increases the reversibility of evolution for small populations that are subject to only modest clonal interference. For small populations, slow switching reduces the mean number of mutations acquired in a new environment and also increases the probability of reverse evolution at each of these “genetic distances.” As the population size increases, slow switching no longer reduces the genetic distance, thus decreasing the evolutionary reversibility. We confirm this effect using both a phenomenological model of clonal interference and also a Wright–Fisher stochastic simulation that incorporates genetic diversity. Our results suggest that the rate of environmental change is a key determinant of the reversibility of evolution, and provides testable hypotheses for experimental evolution.     

Fold or hold: experimental evolution in vitro

We introduce a system for experimental evolution consisting of populations of short oligonucleotides (Oli populations) evolving in a modified quantitative polymerase chain reaction (qPCR). It is tractable at the genetic, genomic, phenotypic and fitness levels. The Oli system uses DNA hairpins designed to form structures that self‐prime under defined conditions. Selection acts on the phenotype of self‐priming, after which differences in fitness are amplified and quantified using qPCR. We outline the methodological and bioinformatics tools for the Oli system here and demonstrate that it can be used as a conventional experimental evolution model system by test‐driving it in an experiment investigating adaptive evolution under different rates of environmental change.     

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.     

Adaptive evolution of lateral plates in three‐spined stickleback Gasterosteus aculeatus: a case study in functional analysis of natural variation

The three‐spined stickleback Gasterosteus aculeatus is a model species for studying questions in ecology and evolution. The rapid diversification of G. aculeatus in post‐glacial freshwater environments, combined with recently developed molecular tools, provides a unique opportunity to study the functional basis of fitness variation in natural populations. In derived freshwater populations, a number of morphological traits have diverged in parallel from the marine ancestral state, including the number of lateral armour plates. Evolution of reduced armour in freshwater populations is due to positive selection from both abiotic and biotic mechanisms. The major effect gene (ectodysplasin‐A or Eda), along with several minor effect genetic regions, has recently been shown to control lateral plate variation. Field experiments have further determined the fitness consequences of allelic variation at the major effect locus. This work helps elucidate the mechanisms connecting genetic variation with phenotypic variation and fitness in the wild, a synthesis that should be applicable to many other phenotypic traits and species of fishes.     

Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution

Experimental microbial evolution has focused on the particular ecological scenario where a population is placed suddenly in an environment where its fitness is low, and then adapts while the environment remains stable. In line with this, most microbial evolution studies use fitness measures that report how evolved genotypes fare when competed directly against their own distant ancestor while other studies compare life history traits (such as growth rates) of ancestral and evolved genotypes. This standard way of measuring and reporting changes in fitness has resulted in a consistent body of literature that explains adaptation when populations evolve in this “standard ecological scenario.” Here, I suggest that for experimental evolution to investigate adaptation in other ecological scenarios, such as fluctuating or persistently changing environments, measures of fitness must be expanded such that they not only continue to be comparable between experiments, but also account for evolution and demographic effects in all environments that an evolving lineage experiences. I examine two non-standard measures of fitness—fitness flux and the total number of reproductive events—as potential ways to quantify adaptation by integrating historical information about selection over many environments. This approach could allow us to make quantitative and biologically-meaningful comparisons of adaptation across diverse ecological scenarios. I use the case study of understanding how phytoplankton communities may respond to global change, where environmental variables change continuously, to explore concrete ways of using non-standard fitness measures that consider both demographic effects and selection in changing, rather than in changed, environments.     

VARIANCE-INDUCED PEAK SHIFTS

The increase in phenotypic variance that occurs in some populations as a result of bottlenecks and founder events can cause a dramatic increase in the probability of a peak shift from one adaptive state to another. Periods of small population size allow drift in the amount of phenotypic variance. Increases in phenotypic variance, coupled with a constant individual fitness function with multiple peaks, can cause the mean fitness landscape to change from bimodal to unimodal, thereby allowing the population's mean phenotype to change deterministically by selection. As the amount of phenotypic variance is returned to an equilibrium state, the multiple peaks reemerge, but the population has moved from one stable state to another. These variance-induced peak shifts allow punctuational evolution from one peak to another at a rate that can be much higher than that predicted by Wright's shifting-balance process alone.     

Natural history collections as windows on evolutionary processes

Natural history collections provide an immense record of biodiversity on Earth. These repositories have traditionally been used to address fundamental questions in biogeography, systematics and conservation. However, they also hold the potential for studying evolution directly. While some of the best direct observations of evolution have come from long‐term field studies or from experimental studies in the laboratory, natural history collections are providing new insights into evolutionary change in natural populations. By comparing phenotypic and genotypic changes in populations through time, natural history collections provide a window into evolutionary processes. Recent studies utilizing this approach have revealed some dramatic instances of phenotypic change over short timescales in response to presumably strong selective pressures. In some instances, evolutionary change can be paired with environmental change, providing a context for potential selective forces. Moreover, in a few cases, the genetic basis of phenotypic change is well understood, allowing for insight into adaptive change at multiple levels. These kinds of studies open the door to a wide range of previously intractable questions by enabling the study of evolution through time, analogous to experimental studies in the laboratory, but amenable to a diversity of species over longer timescales in natural populations.     

Phenotypic responses to temperature in the ciliate Tetrahymena thermophila

Understanding the effects of temperature on ecological and evolutionary processes is crucial for generating future climate adaptation scenarios. Using experimental evolution, we evolved the model ciliate Tetrahymena thermophila in an initially novel high temperature environment for more than 35 generations, closely monitoring population dynamics and morphological changes. We observed initially long lag phases in the high temperature environment that over about 26 generations reduced to no lag phase, a strong reduction in cell size and modifications in cell shape at high temperature. When exposing the adapted populations to their original temperature, most phenotypic traits returned to the observed levels in the ancestral populations, indicating phenotypic plasticity is an important component of this species thermal stress response. However, persistent changes in cell size were detected, indicating possible costs related to the adaptation process. Exploring the molecular basis of thermal adaptation will help clarify the mechanisms driving these phenotypic responses.     

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.