Adapting in larger numbers can increase the vulnerability of Escherichia coli populations to environmental changes

Larger populations generally adapt faster to their existing environment. However, it is unknown if the population size experienced during evolution influences the ability to face sudden environmental changes. To investigate this issue, we subjected replicate Escherichia coli populations of different sizes to experimental evolution in an environment containing a cocktail of three antibiotics. In this environment, the ability to actively efflux molecules outside the cell is expected to be a major fitness‐affecting trait. We found that all the populations eventually reached similar fitness in the antibiotic cocktail despite adapting at different speeds, with the larger populations adapting faster. Surprisingly, although efflux activity (EA) enhanced in the smaller populations, it decayed in the larger ones. The evolution of EA was largely shaped by pleiotropic responses to selection and not by drift. This demonstrates that quantitative differences in population size can lead to qualitative differences (decay/enhancement) in the fate of a character during adaptation to identical environments. Furthermore, the larger populations showed inferior fitness upon sudden exposure to several alternative stressful environments. These observations provide a novel link between population size and vulnerability to environmental changes. Counterintuitively, adapting in larger numbers can render bacterial populations more vulnerable to abrupt environmental changes.     

Alternative responses to rare selection events are differentially vulnerable to changes in the frequency,scope, and intensity of environmental extremes

Extreme weather events are becoming more frequent, severe, and/or widespread as a consequence of anthropogenic climate change. While the economic and ecological implications of these changes have received considerable attention, the role of evolutionary processes in determining organismal responses to these critical challenges is currently unknown. Here we develop a novel theoretical framework that explores how alternative pathways for adaptation to rare selection events can influence population‐level vulnerabilities to future changes in the frequency, scope, and intensity of environmental extremes. We begin by showing that different life histories and trait expression profiles can shift the balance between additive and multiplicative properties of fitness accumulation, favoring different evolutionary responses to identical environmental phenomena. We then demonstrate that these different adaptive outcomes lead to predictable differences in population‐level vulnerabilities to rapid increases in the frequency, intensity, or scope of extreme weather events. Specifically, we show that when the primary mode of fitness accumulation is additive, evolution favors ignoring environmental extremes and lineages become highly vulnerable to extinction if the frequency or scope of extreme weather events suddenly increases. Conversely, when fitness accumulates primarily multiplicatively, evolution favors bet‐hedging phenotypes that cope well with historical extremes and are instead vulnerable to sudden increases in extreme event intensity. Our findings address a critical gap in our understanding of the potential consequences of rare selection events and provide a relatively simple rubric for assessing the vulnerabilities of any population of interest to changes in a wide variety of extreme environmental phenomena.     

Rapid response to changing environments during biological invasions: DNA methylation perspectives

Dissecting complex interactions between species and their environments has long been a research hot spot in the fields of ecology and evolutionary biology. The well‐recognized Darwinian evolution has well‐explained long‐term adaptation scenarios; however, “rapid” processes of biological responses to environmental changes remain largely unexplored, particularly molecular mechanisms such as DNA methylation that have recently been proposed to play crucial roles in rapid environmental adaptation. Invasive species, which have capacities to successfully survive rapidly changing environments during biological invasions, provide great opportunities to study molecular mechanisms of rapid environmental adaptation. Here, we used the methylation‐sensitive amplified polymorphism (MSAP) technique in an invasive model ascidian, Ciona savignyi, to investigate how species interact with rapidly changing environments at the whole‐genome level. We detected quite rapid DNA methylation response: significant changes of DNA methylation frequency and epigenetic differentiation between treatment and control groups occurred only after 1 hr of high‐temperature exposure or after 3 hr of low‐salinity challenge. In addition, we detected time‐dependent hemimethylation changes and increased intragroup epigenetic divergence induced by environmental stresses. Interestingly, we found evidence of DNA methylation resilience, as most stress‐induced DNA methylation variation maintained shortly (~48 hr) and quickly returned back to the control levels. Our findings clearly showed that invasive species could rapidly respond to acute environmental changes through DNA methylation modifications, and rapid environmental changes left significant epigenetic signatures at the whole‐genome level. All these results provide fundamental background to deeply investigate the contribution of DNA methylation mechanisms to rapid contemporary environmental adaptation.     

The evolution of coexistence: Reciprocal adaptation promotes the assembly of a simple community

Species coexistence may result by chance when co‐occurring species do not strongly interact or it may be an evolutionary outcome of strongly interacting species adapting to each other. Although patterns like character displacement indicate that coexistence has often been an evolutionary outcome, it is unclear how often the evolution of coexistence represents adaptation in only one species or reciprocal adaptation among all interacting species. Here, we demonstrate a strong role for evolution in the coexistence of guppies and killifish in Trinidadian streams. We experimentally recreated the temporal stages in the invasion and establishment of guppies into communities that previously contained only killifish. We combined demographic responses of guppies and killifish with a size‐based integral projection model to calculate the fitness of the phenotypes of each species in each of the stages of community assembly. We show that guppies from locally adapted populations that are sympatric with killifish have higher fitness when paired with killifish than guppies from allopatric populations. This elevated fitness involves effects traceable to both guppy and killifish evolution. We discuss the implications of our results to the study of species coexistence and how it may be mediated through eco‐evolutionary feedbacks.     

Predicting patterns of long‐term adaptation and extinction with population genetics

Population genetics struggles to model extinction; standard models track the relative rather than absolute fitness of genotypes, while the exceptions describe only the short‐term transition from imminent doom to evolutionary rescue. But extinction can result from failure to adapt not only to catastrophes, but also to a backlog of environmental challenges. We model long‐term adaptation to long series of small challenges, where fitter populations reach higher population sizes. The population's long‐term fitness dynamic is well approximated by a simple stochastic Markov chain model. Long‐term persistence occurs when the rate of adaptation exceeds the rate of environmental deterioration for some genotypes. Long‐term persistence times are consistent with typical fossil species persistence times of several million years. Immediately preceding extinction, fitness declines rapidly, appearing as though a catastrophe disrupted a stably established population, even though gradual evolutionary processes are responsible. New populations go through an establishment phase where, despite being demographically viable, their extinction risk is elevated. Should the population survive long enough, extinction risk later becomes constant over time.     

ADAPTATION TO DIFFERENT RATES OF ENVIRONMENTAL CHANGE IN CHLAMYDOMONAS

We investigate how different rates of environmental change affect adaptive outcomes and dynamics by selecting Chlamydomonas populations for over 200 generations in environments where the rate of change varies. We find that slower rates of environmental change result in end populations that grow faster and pay a lower cost of adaptation than populations that adapt to a sudden change of the same magnitude. We detected partial selective sweeps in adapting populations by monitoring changes in marker frequency in each population. Although populations adapting to a sudden environmental change showed evidence of mutations of large effect segregating early on, populations adapting to slow rates of change showed patterns that were consistent with mutations of relatively small effect occurring at less predictable times. This work suggests that rates of environmental change may fundamentally alter adaptive dynamics and outcomes of adaptation by changing the size and timing of fitness increases. We suggest that using mutations of smaller effect during adaptation may result in lower levels of pleiotropy and historical constraints, which could in turn result in higher fitness by the end of the experiment.     

ROLE OF SEX AND MIGRATION IN ADAPTATION TO SINK ENVIRONMENTS

Understanding the effects of sex and migration on adaptation to novel environments remains a key problem in evolutionary biology. Using a single‐cell alga Chlamydomonas reinhardtii, we investigated how sex and migration affected rates of evolutionary rescue in a sink environment, and subsequent changes in fitness following evolutionary rescue. We show that sex and migration affect both the rate of evolutionary rescue and subsequent adaptation. However, their combined effects change as the populations adapt to a sink habitat. Both sex and migration independently increased rates of evolutionary rescue, but the effect of sex on subsequent fitness improvements, following initial rescue, changed with migration, as sex was beneficial in the absence of migration but constraining adaptation when combined with migration. These results suggest that sex and migration are beneficial during the initial stages of adaptation, but can become detrimental as the population adapts to its environment.     

Patterns and dynamics of rapid local adaptation and sex in varying habitat types in rotifers

Local adaptation is an important principle in a world of environmental change and might be critical for species persistence. We tested the hypothesis that replicated populations can attain rapid local adaptation under two varying laboratory environments. Clonal subpopulations of the cyclically parthenogenetic rotifer Brachionus calyciflorus were allowed to adapt to two varying harsh and a benign environment: a high‐salt, a food‐limited environment and untreated culture medium (no salt addition, high food). In contrast to most previous studies, we re‐adjusted rotifer density to a fixed value (two individuals per ml) every 3–4 days of unrestricted population growth, instead of exchanging a fixed proportion of the culture medium. Thus our dilution regime specifically selected for high population growth during the entire experiment and it allowed us to continuously track changes in fitness (i.e., maximum population growth under the prevailing conditions) in each population. After 56 days (43 asexual and eight sexual generations) of selection, the populations in the harsh environments showed a significant increase in fitness over time relative to the beginning compared to the population in untreated culture medium. Furthermore, the high‐salt population exhibited a significantly elevated ratio of sexual offspring from the start of the experiment, which suggested that this environment either triggered higher rates of sex or that the untreated medium and the food‐limited environment suppressed sex. In a following assay of local adaptation we measured population fitness under “local” versus “foreign” conditions (populations adapted to this environment compared to those of the other environment) for both harsh habitats. We found significantly higher fitness values for the local populations (on average, a 38% higher fitness) compared to the foreign populations. Overall, local adaptation was formed rapidly and it seemed to be more pronounced in the high‐salt treatment.     

Stress and adaptation in conservation genetics

Stress, adaptation and evolution are major concerns in conservation biology. Stresses from pollution, climatic changes, disease etc. may affect population persistence. Further, stress typically occurs when species are placed in captivity. Threatened species are usually managed to conserve their ability to adapt to environmental changes, whilst species in captivity undergo adaptations that are deleterious upon reintroduction into the wild. In model studies using Drosophila melanogaster, we have found that; (a) inbreeding and loss of genetic variation reduced resistance to the stress of disease, (b) extinction rates under inbreeding are elevated by stress, (c) adaptive evolutionary potential in an increasingly stressful environment is reduced in small population, (d) rates of inbreeding are elevated under stressful conditions, (e) genetic adaptation to captivity reduces fitness when populations are reintroduced into the 'wild', and (f) the deleterious effects of adaptation on reintroduction success can be reduced by population fragmentation.     

Dynamics of molecular evolution in RNA virus populations depend on sudden versus gradual environmental change

Understanding the dynamics of molecular adaptation is a fundamental goal of evolutionary biology. While adaptation to constant environments has been well characterized, the effects of environmental complexity remain seldom studied. One simple but understudied factor is the rate of environmental change. Here we used experimental evolution with RNA viruses to investigate whether evolutionary dynamics varied based on the rate of environmental turnover. We used whole‐genome next‐generation sequencing to characterize evolutionary dynamics in virus populations adapting to a sudden versus gradual shift onto a novel host cell type. In support of theoretical models, we found that when populations evolved in response to a sudden environmental change, mutations of large beneficial effect tended to fix early, followed by mutations of smaller beneficial effect; as predicted, this pattern broke down in response to a gradual environmental change. Early mutational steps were highly parallel across replicate populations in both treatments. The fixation of single mutations was less common than sweeps of associated “cohorts” of mutations, and this pattern intensified when the environment changed gradually. Additionally, clonal interference appeared stronger in response to a gradual change. Our results suggest that the rate of environmental change is an important determinant of evolutionary dynamics in asexual populations.     

Recombination Accelerates Adaptation on a Large-Scale Empirical Fitness Landscape in HIV-1

Recombination has the potential to facilitate adaptation. In spite of the substantial body of theory on the impact of recombination on the evolutionary dynamics of adapting populations, empirical evidence to test these theories is still scarce. We examined the effect of recombination on adaptation on a large-scale empirical fitness landscape in HIV-1 based on in vitro fitness measurements. Our results indicate that recombination substantially increases the rate of adaptation under a wide range of parameter values for population size, mutation rate and recombination rate. The accelerating effect of recombination is stronger for intermediate mutation rates but increases in a monotonic way with the recombination rates and population sizes that we examined. We also found that both fitness effects of individual mutations and epistatic fitness interactions cause recombination to accelerate adaptation. The estimated epistasis in the adapting populations is significantly negative. Our results highlight the importance of recombination in the evolution of HIV-I.     

Cooperation can promote rescue or lead to evolutionary suicide during environmental change

The adaptation of populations to changing conditions may be affected by interactions between individuals. For example, when cooperative interactions increase fecundity, they may allow populations to maintain high densities and thus keep track of moving environmental optima. Simultaneously, changes in population density alter the marginal benefits of cooperative investments, creating a feedback loop between population dynamics and the evolution of cooperation. Here we model how the evolution of cooperation interacts with adaptation to changing environments. We hypothesize that environmental change lowers population size and thus promotes the evolution of cooperation, and that this, in turn, helps the population keep up with the moving optimum. However, we find that the evolution of cooperation can have qualitatively different effects, depending on which fitness component is reduced by the costs of cooperation. If the costs decrease fecundity, cooperation indeed speeds adaptation by increasing population density; if, in contrast, the costs decrease viability, cooperation may instead slow adaptation by lowering the effective population size, leading to evolutionary suicide. Thus, cooperation can either promote or—counterintuitively—hinder adaptation to a changing environment. Finally, we show that our model can also be generalized to other social interactions by discussing the evolution of competition during environmental change.     

Behavioural responses to human‐induced environmental change

The initial response of individuals to human‐induced environmental change is often behavioural. This can improve the performance of individuals under sudden, large‐scale perturbations and maintain viable populations. The response can also give additional time for genetic changes to arise and, hence, facilitate adaptation to new conditions. On the other hand, maladaptive responses, which reduce individual fitness, may occur when individuals encounter conditions that the population has not experienced during its evolutionary history, which can decrease population viability. A growing number of studies find human disturbances to induce behavioural responses, both directly and by altering factors that influence fitness. Common causes of behavioural responses are changes in the transmission of information, the concentration of endocrine disrupters, the availability of resources, the possibility of dispersal, and the abundance of interacting species. Frequent responses are alterations in habitat choice, movements, foraging, social behaviour and reproductive behaviour. Behavioural responses depend on the genetically determined reaction norm of the individuals, which evolves over generations. Populations first respond with individual behavioural plasticity, whereafter changes may arise through innovations and the social transmission of behavioural patterns within and across generations, and, finally, by evolution of the behavioural response over generations. Only a restricted number of species show behavioural adaptations that make them thrive in severely disturbed environments. Hence, rapid human‐induced disturbances often decrease the diversity of native species, while facilitating the spread of invasive species with highly plastic behaviours. Consequently, behavioural responses to human‐induced environmental change can have profound effects on the distribution, adaptation, speciation and extinction of populations and, hence, on biodiversity. A better understanding of the mechanisms of behavioural responses and their causes and consequences could improve our ability to predict the effects of human‐induced environmental change on individual species and on biodiversity.     

Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus

Rapid adaptation can prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics (e.g., rates and patterns of allele frequency change) and genomic basis of successful rescue, particularly in multicellular organisms. We conducted an evolve‐and‐resequence experiment to investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, lentil. Low survival (~1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population, with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. Selection on these loci was only moderately consistent in time, but parallel evolutionary changes were evident in sublines formed after the lentil line had passed through a bottleneck. By comparing estimates of selection and genomic change on lentil across five independent C. maculatus lines (the new lentil‐adapted line, three long‐established lines and one case of failed evolutionary rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary changes. Overall, our results suggest that evolutionary rescue in this system can be caused by very strong selection on multiple loci driving rapid and pronounced genomic change.     

Local adaptation,dispersal evolution,and the spatial eco‐evolutionary dynamics of invasion

Local adaptation and dispersal evolution are key evolutionary processes shaping the invasion dynamics of populations colonizing new environments. Yet their interaction is largely unresolved. Using a single‐species population model along a one‐dimensional environmental gradient, we show how local competition and dispersal jointly shape the eco‐evolutionary dynamics and speed of invasion. From a focal introduction site, the generic pattern predicted by our model features a temporal transition from wave‐like to pulsed invasion. Each regime is driven primarily by local adaptation, while the transition is caused by eco‐evolutionary feedbacks mediated by dispersal. The interaction range and cost of dispersal arise as key factors of the duration and speed of each phase. Our results demonstrate that spatial eco‐evolutionary feedbacks along environmental gradients can drive strong temporal variation in the rate and structure of population spread, and must be considered to better understand and forecast invasion rates and range dynamics.     

The consequences of polyandry for population viability,extinction risk and conservation

Polyandry, by elevating sexual conflict and selecting for reduced male care relative to monandry, may exacerbate the cost of sex and thereby seriously impact population fitness. On the other hand, polyandry has a number of possible population-level benefits over monandry, such as increased sexual selection leading to faster adaptation and a reduced mutation load. Here, we review existing information on how female fitness evolves under polyandry and how this influences population dynamics. In balance, it is far from clear whether polyandry has a net positive or negative effect on female fitness, but we also stress that its effects on individuals may not have visible demographic consequences. In populations that produce many more offspring than can possibly survive and breed, offspring gained or lost as a result of polyandry may not affect population size. Such ecological ‘masking’ of changes in population fitness could hide a response that only manifests under adverse environmental conditions (e.g. anthropogenic change). Surprisingly few studies have attempted to link mating system variation to population dynamics, and in general we urge researchers to consider the ecological consequences of evolutionary processes.     

EFFECTS OF CLIMATE CHANGE ON GLOBAL SEAWEED COMMUNITIES

Seaweeds are ecologically important primary producers, competitors, and ecosystem engineers that play a central role in coastal habitats ranging from kelp forests to coral reefs. Although seaweeds are known to be vulnerable to physical and chemical changes in the marine environment, the impacts of ongoing and future anthropogenic climate change in seaweed‐dominated ecosystems remain poorly understood. In this review, we describe the ways in which changes in the environment directly affect seaweeds in terms of their physiology, growth, reproduction, and survival. We consider the extent to which seaweed species may be able to respond to these changes via adaptation or migration. We also examine the extensive reshuffling of communities that is occurring as the ecological balance between competing species changes, and as top‐down control by herbivores becomes stronger or weaker. Finally, we delve into some of the ecosystem‐level responses to these changes, including changes in primary productivity, diversity, and resilience. Although there are several key areas in which ecological insight is lacking, we suggest that reasonable climate‐related hypotheses can be developed and tested based on current information. By strategically prioritizing research in the areas of complex environmental variation, multiple stressor effects, evolutionary adaptation, and population, community, and ecosystem‐level responses, we can rapidly build upon our current understanding of seaweed biology and climate change ecology to more effectively conserve and manage coastal ecosystems.     

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.     

Mutator dynamics in fluctuating environments

Populations with high mutation rates (mutator clones) are being found in increasing numbers of species, and a clear link is being established between the presence of mutator clones and drug resistance. Mutator clones exist despite the fact that in a constant environment most mutations are deleterious, with the spontaneous mutation rate generally held at a low value. This implies that mutator clones have an important role in the adaptation of organisms to changing environments. Our study examines how mutator dynamics vary according to the frequency of environmental fluctuations. Although recent studies have considered a single environmental switch, here we investigate mutator dynamics in a regularly varying environment, seeking to mimic conditions present, for example, under certain drug or pesticide regimes. Our model provides four significant new insights. First, the results demonstrate that mutators are most prevalent under intermediate rates of environmental change. When the environment oscillates more rapidly, mutators are unable to provide sufficient adaptability to keep pace with the frequent changes in selection pressure and, instead, a population of 'environmental generalists' dominates. Second, our findings reveal that mutator dynamics may be complex, exhibiting limit cycles and chaos. Third, we demonstrate that when each beneficial mutation provides a greater gain in fitness, mutators achieve higher densities in more rapidly fluctuating environments. Fourth, we find that mutators of intermediate strength reach higher densities than very weak or strong mutators.     

Landscape genomic signatures indicate reduced gene flow and forest‐associated adaptive divergence in an endangered neotropical turtle

Human‐induced transformations of ecosystems usually result in fragmented populations subject to increased extinction risk. Fragmentation is also often associated with novel environmental heterogeneity, which in combination with restricted gene flow may increase the opportunity for local adaptation. To manage at‐risk populations in these landscapes, it is important to understand how gene flow is changing, and how populations respond to habitat loss. We conducted a landscape genomics analysis using Restriction‐site Associated DNA sequencing to investigate the evolutionary response of the critically endangered Dahl's Toad‐headed turtle (Mesoclemmys dahli) to severe habitat modification. The species has lost almost all of its natural habitat in the southwestern part of its range and about 70% in the northeast. Based on least cost path analysis across different resistance surfaces for 3,211 SNPs, we found that the landscape matrix is restricting gene flow, causing the fragmentation of the species into at least six populations. Genome scans and allele‐environment association analyses indicate that the population fragments in the deforested grasslands of the southwest are adaptively different from those in the more forested northeast. Populations in areas with no forest had low levels of adaptive genetic diversity and the fixation of ancestrally‐polymorphic SNPs, consistent with directional selection in this novel environment. Our results suggest that this forest‐stream specialist is adapting to pond‐grassland conditions, but it is also suffering from negative consequences of habitat loss, including genetic erosion, isolation, small effective population sizes, and inbreeding. We recommend gene flow restoration via genetic rescue to counteract these threats, and provide guidance for this strategy.