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.     

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.     

Increased susceptibility to fungal disease accompanies adaptation to drought in Brassica rapa

Recent studies have demonstrated adaptive evolutionary responses to climate change, but little is known about how these responses may influence ecological interactions with other organisms, including natural enemies. We used a resurrection experiment in the greenhouse to examine the effect of evolutionary responses to drought on the susceptibility of Brassica rapa plants to a fungal pathogen, Alternaria brassicae. In agreement with previous studies in this population, we found an evolutionary shift to earlier flowering postdrought, which was previously shown to be adaptive. Here, we report the novel finding that postdrought descendant plants were also more susceptible to disease, indicating a rapid evolutionary shift to increased susceptibility. This was accompanied by an evolutionary shift to increased specific leaf area (thinner leaves) following drought. We found that flowering time and disease susceptibility displayed plastic responses to experimental drought treatments, but that this plasticity did not match the direction of evolution, indicating that plastic and evolutionary responses to changes in climate can be opposed. The observed evolutionary shift to increased disease susceptibility accompanying adaptation to drought provides evidence that even if populations can rapidly adapt in response to climate change, evolution in other traits may have ecological effects that could make species more vulnerable.     

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.     

A TEST AND REVIEW OF THE ROLE OF EFFECTIVE POPULATION SIZE ON EXPERIMENTAL SEXUAL SELECTION PATTERNS

Experimental evolution, particularly experimental sexual selection in which sexual selection strength is manipulated by altering the mating system, is an increasingly popular method for testing evolutionary theory. Concerns have arisen regarding genetic diversity variation across experimental treatments: differences in the number and sex ratio of breeders (effective population size; N_e ) and the potential for genetic hitchhiking, both of which may cause different levels of genetic variation between treatments. Such differences may affect the selection response and confound interpretation of results. Here we use both census-based estimators and molecular marker-based estimates to empirically test how experimental evolution of sexual selection in Drosophila pseudoobscura impacts N_e and autosomal genetic diversity. We also consider effects of treatment on X-linked N_e s, which have previously been ignored. Molecular autosomal marker-based estimators indicate that neither N_e nor genetic diversity differs between treatments experiencing different sexual selection intensities; thus observed evolutionary responses reflect selection rather than any confounding effects of experimental design. Given the increasing number of studies on experimental sexual selection, we also review the census N_e s of other experimental systems, calculate X-linked N_e , and compare how different studies have dealt with the issues of inbreeding, genetic drift, and genetic hitchhiking to help inform future designs.     

SIGNAL DESIGN AND PERCEPTION IN HYPOCNEMIS ANTBIRDS: EVIDENCE FOR CONVERGENT EVOLUTION VIA SOCIAL SELECTION

Natural selection is known to produce convergent phenotypes through mimicry or ecological adaptation. It has also been proposed that social selection—i.e., selection exerted by social competition—may drive convergent evolution in signals mediating interspecific communication, yet this idea remains controversial. Here, we use color spectrophotometry, acoustic analyses, and playback experiments to assess the hypothesis of adaptive signal convergence in two competing nonsister taxa, Hypocnemis peruviana and H. subflava (Aves: Thamnophilidae). We show that the structure of territorial songs in males overlaps in sympatry, with some evidence of convergent character displacement. Conversely, nonterritorial vocal and visual signals in males are strikingly diagnostic, in line with 6.8% divergence in mtDNA sequences. The same pattern of variation applies to females. Finally, we show that songs in both sexes elicit strong territorial responses within and between species, whereas songs of a third, allopatric and more closely related species (H. striata) are structurally divergent and elicit weaker responses. Taken together, our results provide compelling evidence that social selection can act across species boundaries to drive convergent or parallel evolution in taxa competing for space and resources.     

Evolution of quantitative traits in the wild: mind the ecology

Recent advances in the quantitative genetics of traits in wild animal populations have created new interest in whether natural selection, and genetic response to it, can be detected within long-term ecological studies. However, such studies have re-emphasized the fact that ecological heterogeneity can confound our ability to infer selection on genetic variation and detect a population''s response to selection by conventional quantitative genetics approaches. Here, I highlight three manifestations of this issue: counter gradient variation, environmentally induced covariance between traits and the correlated effects of a fluctuating environment. These effects are symptomatic of the oversimplifications and strong assumptions of the breeder''s equation when it is applied to natural populations. In addition, methods to assay genetic change in quantitative traits have overestimated the precision with which change can be measured. In the future, a more conservative approach to inferring quantitative genetic response to selection, or genomic approaches allowing the estimation of selection intensity and responses to selection at known quantitative trait loci, will provide a more precise view of evolution in ecological time.     

Genomic signature of natural and anthropogenic stress in wild populations of the waterflea Daphnia magna: validation in space, time and experimental evolution

Natural populations are confronted with multiple selection pressures resulting in a mosaic of environmental stressors at the landscape level. Identifying the genetic underpinning of adaptation to these complex selection environments and assigning causes of natural selection within multidimensional selection regimes in the wild is challenging. The water flea Daphnia is a renowned ecological model system with its well-documented ecology, the possibility to analyse subfossil dormant egg banks and the short generation time allowing an experimental evolution approach. Capitalizing on the strengths of this model system, we here link candidate genome regions to three selection pressures, known to induce micro-evolutionary responses in Daphnia magna: fish predation, parasitism and land use. Using a genome scan approach in space, time and experimental evolution trials, we provide solid evidence of selection at the genome level under well-characterized environmental gradients in the wild and identify candidate genes linked to the three environmental stressors. Our study reveals differential selection at the genome level in Daphnia populations and provides evidence for repeatable patterns of local adaptation in a geographic mosaic of environmental stressors fuelled by standing genetic variation. Our results imply high evolutionary potential of local populations, which is relevant to understand the dynamics of trait changes in natural populations and their impact on community and ecosystem responses through eco-evolutionary feedbacks.     

Effects of prior exposure to antibiotics on bacterial adaptation to phages

Understanding adaptation to complex environments requires information about how exposure to one selection pressure affects adaptation to others. For bacteria, antibiotics and viral parasites (phages) are two of the most common selection pressures and are both relevant for treatment of bacterial infections: increasing antibiotic resistance is generating significant interest in using phages in addition or as an alternative to antibiotics. However, we lack knowledge of how exposure to antibiotics affects bacterial responses to phages. Specifically, it is unclear how the negative effects of antibiotics on bacterial population growth combine with any possible mutagenic effects or physiological responses to influence adaptation to other stressors such as phages, and how this net effect varies with antibiotic concentration. Here, we experimentally addressed the effect of pre‐exposure to a wide range of antibiotic concentrations on bacterial responses to phages. Across 10 antibiotics, we found a strong association between their effects on bacterial population size and subsequent population growth in the presence of phages (which in these conditions indicates phage‐resistance evolution). We detected some evidence of mutagenesis among populations treated with fluoroquinolones and β‐lactams at sublethal doses, but these effects were small and not consistent across phage treatments. These results show that, although stressors such as antibiotics can boost adaptation to other stressors at low concentrations, these effects are weak compared to the effect of reduced population growth at inhibitory concentrations, which in our experiments strongly reduced the likelihood of subsequent phage‐resistance evolution.     

Triangulating the genetic basis of adaptation to multifarious selection

Understanding how natural populations adapt to their local environments is a major research theme for ecological genomics. This endeavour begins by sleuthing for shared genetic similarities among unrelated natural populations sharing adaptive traits to documented selective pressures. When the selective pressures have low dimensionality, and the genetic response is localized to a few genes of major effect, this detective work is relatively straightforward. However, in the real world, populations face a complex mixture of selective pressures and many adaptive responses are the result of changes in quantitative traits that have a polygenic genetic basis. This complex relationship between environment and adaptation presents a significant challenge. How can we begin to identify drivers of adaptation in natural settings? In this issue of Molecular Ecology, Orsini et al. (2012) take advantage of the biological attributes of the freshwater microcrustacean Daphnia ( Fig. 1 ) to disentangle multidimensional selection’s signature on the genome of populations that have repeatedly evolved adaptive responses to isolated selective pressures including predation, parasitism and anthropogenic changes in land use. Orsini et al. (2012) leverage a powerful combination of spatially structured populations in a geographic mosaic of environmental stressors, the historical archive of past genotypes preserved in lake‐bottom sediments and selection experiments to identify sets of candidate genomic regions associated with adaptation in response to these three environmental stressors. This study provides a template for future investigation in ecological genomics, combining multiple experimental approaches with the genomic investigation of a well‐studied ecological model species.

Figure 1 Open in figure viewer PowerPoint Adult Daphnia magna carrying a resting egg in the brood pouch. The water flea Daphnia is a renowned ecological model system and rapidly developing as an ecological and environmental genomics model species. Photo credit Joachim Mergeay.     

Experimental evolution in Drosophila melanogaster: interaction of temperature and food quality selection regimes

Abstract. In Drosophila , both the phenotypic and evolutionary effect of temperature on adult size involves alterations to larval resource processing and affects other life-history traits, that is, development time but most notably, larval survival. Therefore, thermal evolution of adult body size might not be independent of simultaneous adaptation of larval traits to resource availability. Using experimental evolution lines adapted to high and low temperatures at different levels of food, we show that selection pressures interact in shaping larval resource processing. Evolution on poor food invariably leads to lower resource acquisition suggesting a cost to feeding behavior. However, following low temperature selection, lower resource acquisition led to a higher adult body size, probably by more efficient allocation to growth. In contrast, following high temperature selection, low resource acquisition benefited larval survival, possibly by reducing feeding-associated costs. We show that evolved differences to larval resource processing provide a possible proximate mechanism to variation in a suite of correlated life-history traits during adaptation to different climates. The implication for natural populations is that in nature, thermal evolution drives populations to opposite ends of an adult size versus larval survival trade-off by altering resource processing, if resource availability is limited.     

Parallel genotypic adaptation: when evolution repeats itself

Until recently, parallel genotypic adaptation was considered unlikely because phenotypic differences were thought to be controlled by many genes. There is increasing evidence, however, that phenotypic variation sometimes has a simple genetic basis and that parallel adaptation at the genotypic level may be more frequent than previously believed. Here, we review evidence for parallel genotypic adaptation derived from a survey of the experimental evolution, phylogenetic, and quantitative genetic literature. The most convincing evidence of parallel genotypic adaptation comes from artificial selection experiments involving microbial populations. In some experiments, up to half of the nucleotide substitutions found in independent lineages under uniform selection are the same. Phylogenetic studies provide a means for studying parallel genotypic adaptation in non-experimental systems, but conclusive evidence may be difficult to obtain because homoplasy can arise for other reasons. Nonetheless, phylogenetic approaches have provided evidence of parallel genotypic adaptation across all taxonomic levels, not just microbes. Quantitative genetic approaches also suggest parallel genotypic evolution across both closely and distantly related taxa, but it is important to note that this approach cannot distinguish between parallel changes at homologous loci versus convergent changes at closely linked non-homologous loci. The finding that parallel genotypic adaptation appears to be frequent and occurs at all taxonomic levels has important implications for phylogenetic and evolutionary studies. With respect to phylogenetic analyses, parallel genotypic changes, if common, may result in faulty estimates of phylogenetic relationships. From an evolutionary perspective, the occurrence of parallel genotypic adaptation provides increasing support for determinism in evolution and may provide a partial explanation for how species with low levels of gene flow are held together.     

Adaptation to developmental diet influences the response to selection on age at reproduction in the fruit fly

Experimental evolution (EE) is a powerful tool for addressing how environmental factors influence life‐history evolution. While in nature different selection pressures experienced across the lifespan shape life histories, EE studies typically apply selection pressures one at a time. Here, we assess the consequences of adaptation to three different developmental diets in combination with classical selection for early or late reproduction in the fruit fly Drosophila melanogaster. We find that the response to each selection pressure is similar to that observed when they are applied independently, but the overall magnitude of the response depends on the selection regime experienced in the other life stage. For example, adaptation to increased age at reproduction increased lifespan across all diets; however, the extent of the increase was dependent on the dietary selection regime. Similarly, adaptation to a lower calorie developmental diet led to faster development and decreased adult weight, but the magnitude of the response was dependent on the age‐at‐reproduction selection regime. Given that multiple selection pressures are prevalent in nature, our findings suggest that trade‐offs should be considered not only among traits within an organism, but also among adaptive responses to different—sometimes conflicting—selection pressures, including across life stages.     

The evolution of quantitative traits in complex environments

Species inhabit complex environments and respond to selection imposed by numerous abiotic and biotic conditions that vary in both space and time. Environmental heterogeneity strongly influences trait evolution and patterns of adaptive population differentiation. For example, heterogeneity can favor local adaptation, or can promote the evolution of plastic genotypes that alter their phenotypes based on the conditions they encounter. Different abiotic and biotic agents of selection can act synergistically to either accelerate or constrain trait evolution. The environmental context has profound effects on quantitative genetic parameters. For instance, heritabilities measured in controlled conditions often exceed those measured in the field; thus, laboratory experiments could overestimate the potential for a population to respond to selection. Nevertheless, most studies of the genetic basis of ecologically relevant traits are conducted in simplified laboratory environments, which do not reflect the complexity of nature. Here, we advocate for manipulative field experiments in the native ranges of plant species that differ in mating system, life-history strategy and growth form. Field studies are vital to evaluate the roles of disparate agents of selection, to elucidate the targets of selection and to develop a nuanced perspective on the evolution of quantitative traits. Quantitative genetics field studies will also shed light on the potential for natural populations to adapt to novel climates in highly fragmented landscapes. Drawing from our experience with the ecological model system Boechera (Brassicaceae), we discuss advancements possible through dedicated field studies, highlight future research directions and examine the challenges associated with field studies.     

Adaptation and habitat selection in the eco-evolutionary process

The struggle for existence occurs through the vital rates of population growth. This basic fact demonstrates the tight connection between ecology and evolution that defines the emerging field of eco-evolutionary dynamics. An effective synthesis of the interdependencies between ecology and evolution is grounded in six principles. The mechanics of evolution specifies the origin and rules governing traits and evolutionary strategies. Traits and evolutionary strategies achieve their selective value through their functional relationships with fitness. Function depends on the underlying structure of variation and the temporal, spatial and organizational scales of evolution. An understanding of how changes in traits and strategies occur requires conjoining ecological and evolutionary dynamics. Adaptation merges these five pillars to achieve a comprehensive understanding of ecological and evolutionary change. I demonstrate the value of this world-view with reference to the theory and practice of habitat selection. The theory allows us to assess evolutionarily stable strategies and states of habitat selection, and to draw the adaptive landscapes for habitat-selecting species. The landscapes can then be used to forecast future evolution under a variety of climate change and other scenarios.     

ADAPTATION TO DESICCATION FAILS TO GENERATE PRE‐ AND POSTMATING ISOLATION IN REPLICATE DROSOPHILA MELANOGASTER LABORATORY POPULATIONS

Many laboratory speciation experiments have raised allopatric populations in different environments to determine whether reproductive isolation evolves as a byproduct of adaptation (a form of ecological speciation). Few, however, have addressed the evolution of both pre‐ and postmating isolation or investigated the conditions affecting the process. We present results of an evolution experiment in which 12 lines of Drosophila melanogaster were derived from a common population and then independently evolved for more than 57 generations under alternative selection treatments. Six “desiccation” populations had access to food and water removed during a period of their adult lives generating strong desiccation selection, and six “starvation” populations had access to food but not water removed for the same period, generating a mild starvation stress. Substantial divergence of cuticular hydrocarbons occurred between the desiccation and starvation populations, key traits that have been implicated in sexual isolation in Drosophila. Despite this divergence, there was no detectable premating isolation between desiccation and starvation populations and postmating isolation was asymmetrical: the fitness of F1 hybrids was reduced in the desiccation but not the starvation environment. This asymmetry was likely caused by the absence of divergent selection: adaptation to desiccation appears to have come at no cost to performance in the starvation environment. Novel environments are thought to promote the evolution of reproductive isolation. Understanding the conditions that favor or hamper this remains a key challenge for speciation research.     

Rapid evolution of cold tolerance in stickleback

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.     

Direct and correlated responses to artificial selection on sexual size dimorphism in the flour beetle, Tribolium castaneum

Sexual size dimorphism (SSD) is a conspicuous yet poorly understood pattern across many organisms. Although artificial selection is an important tool for studying the evolution of SSD, previous studies have applied selection to only a single sex or to both sexes in the same direction. In nature, however, SSD likely arises through sex-specific selection on body size. Here, we use Tribolium castaneum flour beetles to investigate the evolution of SSD by subjecting males and females to sexually antagonistic selection on body size (sexes selected in opposite directions). Additionally, we examined correlated responses to body size selection in larval growth rates and development time. After seven generations, SSD remained unchanged in all selected lines; this observed lack of response to short-term selection may be attributed to evolutionary constraints arising from between-sex body size correlations. Developmental traits showed complex correlated responses under different selection treatments. These results suggest that sex-specific larval development patterns may facilitate the evolution of SSD.     

陆地生态系统环境控制实验的研究方法及技术体系

生物及生态系统与环境变化间的反馈关系及其过程机制是生态学研究的重要内容。不同类型的生物环境因素控制实验以及大尺度的联网野外控制实验被认为是认识生态系统响应和适应环境变化过程机制、精细定量表达的有效手段及认知过程的加速器。近年来发展了大型野外物理模拟实验装置网络(如ECOTRON)、生态系统分析与实验平台(AnaEE)、国际干旱实验研究网络(Drought Network)、氮沉降联合实验网络(Nutrient Network),以及基于各区域性生态观测实验站的联网控制实验(如USA-ILTER)。发展大陆尺度联网实验研究平台事业正日益受到学术界的重视,将会在认知生态系统环境响应过程机制方面发挥更重要的作用。基于以上背景,本文综述了生态系统环境控制实验的研究方法和实验体系的发展,明确指出各种类型的生物环境控制实验需要形成联合协作体系,共同解决生态系统对环境变化的响应及适应的基本科学问题。目前的控制实验包括: 1) 实验室封闭装置内的生物生理生态学控制实验;2) 野外实验场的半开放部分环境要素控制实验;3) 近自然状态的野外环境控制实验;以及4) 基于野外生态站的联网控制实验。进而,本文还深入讨论了陆地生态系统的环境响应及适应过程机制实验系统设计的发展趋势,分析了基于大尺度自然环境梯度实验及生态站尺度的要素控制实验的优势,提出了整合两种实验技术、发展新一代的野外联网实验体系的科学设想,讨论了基于野外联网控制实验的研究体系,论证了研究生态系统对环境变化短期响应和长期适应的规律和机制、生态系统环境响应定量表达的技术途径。若本文提出的控制实验体系设计方案能够得以实施,必将大大促进我国乃至全球生态系统和环境变化科学的研究水平,对我国应对气候变化和生态环境建设具有重要的科学意义。