Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics

CONTENTS: Summary 752 I. Introduction 752 II. Will migration be enough? 753 III. Can adaptation proceed fast enough? 754 IV. Fitness links demographic and evolutionary processes 755 V. Experimental studies: what do they tell us and how can we improve them? 756 VI. Predicting evolutionary change based on genetic variation and natural selection 757 VII. The chronosequence approach 758 VIII. Resurrection of ancestral propagules 759 IX. The mean and variance in fitness, a link between genetics and demography 760 X. Conclusions 762 Acknowledgements 762 References 762 SUMMARY: Evolution proceeds unceasingly in all biological populations. It is clear that climate-driven evolution has molded plants in deep time and within extant populations. However, it is less certain whether adaptive evolution can proceed sufficiently rapidly to maintain the fitness and demographic stability of populations subjected to exceptionally rapid contemporary climate change. Here, we consider this question, drawing on current evidence on the rate of plant range shifts and the potential for an adaptive evolutionary response. We emphasize advances in understanding based on theoretical studies that model interacting evolutionary processes, and we provide an overview of quantitative genetic approaches that can parameterize these models to provide more meaningful predictions of the dynamic interplay between genetics, demography and evolution. We outline further research that can clarify both the adaptive potential of plant populations as climate continues to change and the role played by ongoing adaptation in their persistence.     

The effect of sex on the mean and variance of fitness in facultatively sexual rotifers

The evolution of sex is a classic problem in evolutionary biology. While this topic has been the focus of much theoretical work, there is a serious dearth of empirical data. A simple yet fundamental question is how sex affects the mean and variance in fitness. Despite its importance to the theory, this type of data is available for only a handful of taxa. Here, we report two experiments in which we measure the effect of sex on the mean and variance in fitness in the monogonont rotifer, Brachionus calyciflorus. Compared to asexually derived offspring, we find that sexual offspring have lower mean fitness and less genetic variance in fitness. These results indicate that, at least in the laboratory, there are both short- and long-term disadvantages associated with sexual reproduction. We briefly review the other available data and highlight the need for future work.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Evolution in response to climate change: In pursuit of the missing evidence

Climate change is imposing intensified and novel selection pressures on organisms by altering abiotic and biotic environmental conditions on Earth, but studies demonstrating genetic adaptation to climate change mediated selection are still scarce. Evidence is accumulating to indicate that both genetic and ecological constrains may often limit populations' abilities to adapt to large scale effects of climate warming. These constraints may predispose many organisms to respond to climate change with range shifts and phenotypic plasticity, rather than through evolutionary adaptation. In general, broad conclusions about the role of evolutionary adaptation in mitigating climate change induced fitness loss in the wild are as yet difficult to make. Editor's suggested further reading in BioEssays: How will fish that evolved at constant sub‐zero temperatures cope with global warming? Notothenioids as a case study Abstract     

Formal Darwinism

Two questions are raised for Grafen’s formal darwinism project of aligning evolutionary dynamics under natural selection with the optimization of phenotypes for individuals of a population. The first question concerns mean fitness maximization during frequency-dependent selection; in such selection regimes, not only is mean fitness typically not maximized but it is implausible that any parameter closely related to fitness is being maximized. The second question concerns whether natural selection on inclusive fitness differences can be regarded as individual selection or whether it leads to a departure from the central motivation that led to the formal darwinism project, viz., to show that “Darwinian” evolution through individual selection leads to “good design” or phenotypic adaptation through trait optimization.     

Beneficial fitness effects are not exponential for two viruses

The distribution of fitness effects for beneficial mutations is of paramount importance in determining the outcome of adaptation. It is generally assumed that fitness effects of beneficial mutations follow an exponential distribution, for example, in theoretical treatments of quantitative genetics, clonal interference, experimental evolution, and the adaptation of DNA sequences. This assumption has been justified by the statistical theory of extreme values, because the fitnesses conferred by beneficial mutations should represent samples from the extreme right tail of the fitness distribution. Yet in extreme value theory, there are three different limiting forms for right tails of distributions, and the exponential describes only those of distributions in the Gumbel domain of attraction. Using beneficial mutations from two viruses, we show for the first time that the Gumbel domain can be rejected in favor of a distribution with a right-truncated tail, thus providing evidence for an upper bound on fitness effects. Our data also violate the common assumption that small-effect beneficial mutations greatly outnumber those of large effect, as they are consistent with a uniform distribution of beneficial effects.     

The evolution of mutation rate in finite asexual populations

In this article, we model analytically the evolution of mutation rate in asexual organisms. Three selective forces are present. First, everything else being equal, individuals with higher mutation rate have a larger fitness, thanks to the energy and time saved by not replicating DNA accurately. Second, as a flip side, the genome of these individuals is replicated with errors that may negatively affect fitness. Third, and conversely, replication errors have a potential benefit if beneficial mutations are to be generated. Our model describes the fate of modifiers of mutation rate under the three forces and allows us to predict the long-term evolutionary trajectory of mutation rate. We obtain three major results. First, in asexuals, the needs for both adaptation and genome preservation are not evolutionary forces that can stabilize mutation rate at an intermediate optimum. When adaptation has a significant role, it primarily destabilizes mutation rate and yields the emergence of strong-effect mutators. Second, in contrast to what is usually believed, the appearance of modifiers with large mutation rate is more likely when the fitness cost of each deleterious mutation is weak, because the cost of replication errors is then paid after a delay. Third, in small populations, and even if adaptations are needed, mutation rate is always blocked at the minimum attainable level, because the rate of adaptation is too slow to play a significant role. Only populations whose size is above a critical mass see their mutation rate affected by the need for adaptation.     

Theoretical biology in the third millennium

During the 20th century our understanding of genetics and the processes of gene expression have undergone revolutionary change. Improved technology has identified the components of the living cell, and knowledge of the genetic code allows us to visualize the pathway from genotype to phenotype. We can now sequence entire genes, and improved cloning techniques enable us to transfer genes between organisms, giving a better understanding of their function. Due to the improved power of analytical tools databases of sequence information are growing at an exponential rate. Soon complete sequences of genomes and the three-dimensional structure of all proteins may be known. The question we face in the new millennium is how to apply this data in a meaningful way. Since the genes carry the specification of an organism, and because they also record evolutionary changes, we need to design a theoretical framework that can take account of the flow of information through biological systems.     

The genetic basis of thermal reaction norm evolution in lab and natural phage populations

Two major goals of laboratory evolution experiments are to integrate from genotype to phenotype to fitness, and to understand the genetic basis of adaptation in natural populations. Here we demonstrate that both goals are possible by re-examining the outcome of a previous laboratory evolution experiment in which the bacteriophage G4 was adapted to high temperatures. We quantified the evolutionary changes in the thermal reaction norms—the curves that describe the effect of temperature on the growth rate of the phages—and decomposed the changes into modes of biological interest. Our analysis indicated that changes in optimal temperature accounted for almost half of the evolutionary changes in thermal reaction norm shape, and made the largest contribution toward adaptation at high temperatures. Genome sequencing allowed us to associate reaction norm shape changes with particular nucleotide mutations, and several of the identified mutations were found to be polymorphic in natural populations. Growth rate measures of natural phage that differed at a site that contributed substantially to adaptation in the lab indicated that this mutation also underlies thermal reaction norm shape variation in nature. In combination, our results suggest that laboratory evolution experiments may successfully predict the genetic bases of evolutionary responses to temperature in nature. The implications of this work for viral evolution arise from the fact that shifts in the thermal optimum are characterized by tradeoffs in performance between high and low temperatures. Optimum shifts, if characteristic of viral adaptation to novel temperatures, would ensure the success of vaccine development strategies that adapt viruses to low temperatures in an attempt to reduce virulence at higher (body) temperatures.     

Genetics, development and evolution of adaptive pigmentation in vertebrates

The study of pigmentation has played an important role in the intersection of evolution, genetics, and developmental biology. Pigmentation's utility as a visible phenotypic marker has resulted in over 100 years of intense study of coat color mutations in laboratory mice, thereby creating an impressive list of candidate genes and an understanding of the developmental mechanisms responsible for the phenotypic effects. Variation in color and pigment patterning has also served as the focus of many classic studies of naturally occurring phenotypic variation in a wide variety of vertebrates, providing some of the most compelling cases for parallel and convergent evolution. Thus, the pigmentation model system holds much promise for understanding the nature of adaptation by linking genetic changes to variation in fitness-related traits. Here, I first discuss the historical role of pigmentation in genetics, development and evolutionary biology. I then discuss recent empirically based studies in vertebrates, which rely on these historical foundations to make connections between genotype and phenotype for ecologically important pigmentation traits. These studies provide insight into the evolutionary process by uncovering the genetic basis of adaptive traits and addressing such long-standing questions in evolutionary biology as (1) are adaptive changes predominantly caused by mutations in regulatory regions or coding regions? (2) is adaptation driven by the fixation of dominant mutations? and (3) to what extent are parallel phenotypic changes caused by similar genetic changes? It is clear that coloration has much to teach us about the molecular basis of organismal diversity, adaptation and the evolutionary process.     

Sulfur Isotope Fractionation during the Evolutionary Adaptation of a Sulfate-Reducing Bacterium

Dissimilatory sulfate reduction is a microbial catabolic pathway that preferentially processes less massive sulfur isotopes relative to their heavier counterparts. This sulfur isotope fractionation is recorded in ancient sedimentary rocks and generally is considered to reflect a phenotypic response to environmental variations rather than to evolutionary adaptation. Modern sulfate-reducing microorganisms isolated from similar environments can exhibit a wide range of sulfur isotope fractionations, suggesting that adaptive processes influence the sulfur isotope phenotype. To date, the relationship between evolutionary adaptation and isotopic phenotypes has not been explored. We addressed this by studying the covariation of fitness, sulfur isotope fractionation, and growth characteristics in Desulfovibrio vulgaris Hildenborough in a microbial evolution experiment. After 560 generations, the mean fitness of the evolved lineages relative to the starting isogenic population had increased by ∼17%. After 927 generations, the mean fitness relative to the initial ancestral population had increased by ∼20%. Growth rate in exponential phase increased during the course of the experiment, suggesting that this was a primary influence behind the fitness increases. Consistent changes were observed within different selection intervals between fractionation and fitness. Fitness changes were associated with changes in exponential growth rate but changes in fractionation were not. Instead, they appeared to be a response to changes in the parameters that govern growth rate: yield and cell-specific sulfate respiration rate. We hypothesize that cell-specific sulfate respiration rate, in particular, provides a bridge that allows physiological controls on fractionation to cross over to the adaptive realm.     

Distributions of beneficial fitness effects in RNA

Beneficial mutations are the driving force of evolution by natural selection. Yet, relatively little is known about the distribution of the fitness effects of beneficial mutations in populations. Recent work of Gillespie and Orr suggested some of the first generalizations for the distributions of beneficial fitness effects and, surprisingly, they depend only weakly on biological details. In particular, the theory suggests that beneficial mutations obey an exponential distribution of fitness effects, with the same exponential parameter across different regions of genotype space, provided only that few possible beneficial mutations are available to that genotype. Here we tested this hypothesis with a quasi-empirical model of RNA evolution in which fitness is based on the secondary structures of molecules and their thermodynamic stabilities. The fitnesses of randomly selected genotypes appeared to follow a Gumbel-type distribution and thus conform to a basic assumption of adaptation theory. However, the observed distributions of beneficial fitness effects conflict with specific predictions of the theory. In particular, the distributions of beneficial fitness effects appeared exponential only when the vast majority of small-effect beneficial mutations were ignored. Additionally, the distribution of beneficial fitness effects varied with the fitness of the parent genotype. We believe that correlation of the fitness values among similar genotypes is likely the cause of the departure from the predictions of recent adaptation theory. Although in conflict with the current theory, these results suggest that more complex statistical generalizations about beneficial mutations may be possible.     

A generalised approach to the study and understanding of adaptive evolution

Evolutionary theory has made large impacts on our understanding and management of the world, in part because it has been able to incorporate new data and new insights successfully. Nonetheless, there is currently a tension between certain biological phenomena and mainstream evolutionary theory. For example, how does the inheritance of molecular epigenetic changes fit into mainstream evolutionary theory? Is niche construction an evolutionary process? Is local adaptation via habitat choice also adaptive evolution? These examples suggest there is scope (and perhaps even a need) to broaden our views on evolution. We identify three aspects whose incorporation into a single framework would enable a more generalised approach to the understanding and study of adaptive evolution: (i) a broadened view of extended phenotypes; (ii) that traits can respond to each other; and (iii) that inheritance can be non-genetic. We use causal modelling to integrate these three aspects with established views on the variables and mechanisms that drive and allow for adaptive evolution. Our causal model identifies natural selection and non-genetic inheritance of adaptive parental responses as two complementary yet distinct and independent drivers of adaptive evolution. Both drivers are compatible with the Price equation; specifically, non-genetic inheritance of parental responses is captured by an often-neglected component of the Price equation. Our causal model is general and simplified, but can be adjusted flexibly in terms of variables and causal connections, depending on the research question and/or biological system. By revisiting the three examples given above, we show how to use it as a heuristic tool to clarify conceptual issues and to help design empirical research. In contrast to a gene-centric view defining evolution only in terms of genetic change, our generalised approach allows us to see evolution as a change in the whole causal structure, consisting not just of genetic but also of phenotypic and environmental variables.     

Genomic biodiversity, phylogenetics and coevolution in proteins

Comprehensive sampling of genomic biodiversity is fast becoming a reality for some genomic regions and complete organelle genomes. Genomic biodiversity is defined as large genomic sequences from many species, and here some recent work is reviewed that demonstrates the potential benefits of genomic biodiversity for molecular evolutionary analysis and phylogenetic reconstruction. This work shows that using likelihood-based approaches, taxon addition can dramatically improve phylogenetic reconstruction. Features or dynamics of the evolutionary process are much more easily inferred with large numbers of taxa, and large numbers are essential for discriminating differences in evolutionary patterns between sites. Accurate prediction of site-specific patterns can improve phylogenetic reconstruction by an amount equivalent to quadrupling sequence length. Genomic biodiversity is particularly central to research relating patterns of evolution, adaptation and coevolution to structural and functional features of proteins. Research on detecting coevolution between amino acid residues in proteins demonstrates a clear need for much greater numbers of closely related taxa to better discriminate site-specific patterns of interaction, and to allow more detailed analysis of coevolutionary interactions between subunits in protein complexes. It is argued that parsing out coevolutionary and other context-dependent substitution probabilities is essential for discriminating between coevolution and adaptation, and for more realistically modelling the evolution of proteins. Also reviewed is research that argues for increasing the efficiency of acquiring genomic biodiversity, and suggests that this might be done by simultaneously shotgun cloning and sequencing genomic mixtures from many species. Increased efficiency is a prerequisite if genomic biodiversity levels are to rapidly increase by orders of magnitude, and thus lead to dramatically improved understanding of interactions between protein structure, function and sequence evolution.     

The hormetic zone: an ecological and evolutionary perspective based upon habitat characteristics and fitness selection.

Fitness varies nonlinearly with environmental variables such as temperature, water availability, and nutrition, with maximum fitness at intermediate levels between more stressful extremes. For environmental agents that are highly toxic at exposures that substantially exceed background levels, fitness is maximized at concentrations near zero--a phenomenon often referred to as hormesis. Two main components are suggested: (1) background hormesis, which derives from the direct adaptation of organisms to their habitats; and (2) stress-derived hormonesis, which derives from metabolic reserves that are maintained as an adaptation to environmental stresses through evolutionary time. These reserves provide protection from lesser correlated stresses. This article discusses illustrative examples, including ethanol and ionizing radiation, aimed at placing hormesis into an ecological and evolutionary context. A unifying approach comes from fitness-stress continua that underlie responses to abiotic variables, whereby selection for maximum metabolic efficiency and hence fitness in adaptation to habitats in nature underlies hormetic zones. Within this reductionist model, more specific metabolic mechanisms to explain hormesis are beginning to emerge, depending upon the agent and the taxon in question. Some limited research possibilities based upon this evolutionary perspective are indicated.     

Efficient algorithms for protein sequence design and the analysis of certain evolutionary fitness landscapes.

Protein sequence design is a natural inverse problem to protein structure prediction: given a target structure in three dimensions, we wish to design an amino acid sequence that is likely fold to it. A model of Sun, Brem, Chan, and Dill casts this problem as an optimization on a space of sequences of hydrophobic (H) and polar (P) monomers; the goal is to find a sequence that achieves a dense hydrophobic core with few solvent-exposed hydrophobic residues. Sun et al. developed a heuristic method to search the space of sequences, without a guarantee of optimality or near-optimality; Hart subsequently raised the computational tractability of constructing an optimal sequence in this model as an open question. Here we resolve this question by providing an efficient algorithm to construct optimal sequences; our algorithm has a polynomial running time, and performs very efficiently in practice. We illustrate the implementation of our method on structures drawn from the Protein Data Bank. We also consider extensions of the model to larger amino acid alphabets, as a way to overcome the limitations of the binary H/P alphabet. We show that for a natural class of arbitrarily large alphabets, it remains possible to design optimal sequences efficiently. Finally, we analyze some of the consequences of this sequence design model for the study of evolutionary fitness landscapes. A given target structure may have many sequences that are optimal in the model of Sun et al.; following a notion raised by the work of J. Maynard Smith, we can ask whether these optimal sequences are "connected" by successive point mutations. We provide a polynomial-time algorithm to decide this connectedness property, relative to a given target structure. We develop the algorithm by first solving an analogous problem expressed in terms of submodular functions, a fundamental object of study in combinatorial optimization.     

Brave New World: the epistatic foundations of natives adapting to invaders

Classical examples indicated rapid evolution to be both rare and largely anthropogenic. As the pace and scale of human disturbance increase, such evolution is becoming more the norm. Genetically based adaptation may underlie successful biological invasions, and may likewise characterize responses in natives to invasives. Recent published studies confirm that natives are adapting morphologically, behaviorally, physiologically and life historically to selection from invasive species. Some of the processes involved are evident in our studies of recent host shifts to invasive plants by native soapberry bugs in North America and Australia. On both continents populations have differentiated extensively in fitness traits. Genetic architecture of these adaptations involves a surprising degree of non-additive variation (epistasis, dominance), a result that in theory may reflect a history of colonization by a small number of individuals followed by population growth. Such “founder-flush” events may unleash extraordinary evolutionary potential, and their importance will be clarified as more studies take advantage of the accidental perturbation experiments that biotic invasions represent. From a conservation standpoint, rapid evolution in natives will present challenges for ecologically appropriate and sustainable management, but at the same time may enhance the capacity of the native community to act in the biological control of invasive species.     

Entropy increase and information loss in Markov models of evolution

Markov models of evolution describe changes in the probability distribution of the trait values a population might exhibit. In consequence, they also describe how entropy and conditional entropy values evolve, and how the mutual information that characterizes the relation between an earlier and a later moment in a lineage’s history depends on how much time separates them. These models therefore provide an interesting perspective on questions that usually are considered in the foundations of physics—when and why does entropy increase and at what rates do changes in entropy take place? They also throw light on an important epistemological question: are there limits on what your observations of the present can tell you about the evolutionary past?     

Contributions of domesticated plant studies to our understanding of plant evolution

BACKGROUND: Plant evolutionary theory has been greatly enriched by studies on crop species. Over the last century, important information has been generated on many aspects of population biology, speciation and polyploid genetics. SCOPE: Searches for quantitative trait loci (QTL) in crop species have uncovered numerous blocks of genes that have dramatic effects on adaptation, particularly during the domestication process. Many of these QTL have epistatic and pleiotropic effects making rapid evolutionary change possible. Most of the pioneering work on the molecular basis of self-incompatibility has been conducted on crop species, along with the sequencing of the phytopathogenic resistance genes (R genes) responsible for the 'gene-to-gene' relations of coevolution observed in host-pathogen relationships. Some of the better examples of co-adaptation and early acting inbreeding depression have also been elucidated in crops. Crop-wild progenitor interactions have provided rich opportunities to study the evolution of novel adaptations subsequent to hybridization. Most crop/wild F1 hybrids have reduced fitness, but in some instances the crop relatives have acquired genes that make them more efficient weeds through crop mimicry. Studies on autopolyploid alfalfa and potato have uncovered the means by which polyploid gametes are formed and have led to hypotheses about how multiallelic interactions are associated with fitness and self-fertility. Research on the cole crops and wheat has discovered that newly formed polyploids can undergo dramatic genome rearrangements that could lead to rapid evolutionary change. CONCLUSIONS: Many more important evolutionary discoveries are on the horizon, now that the whole genome sequence is available of the two major subspecies of rice Oryza sativa ssp. japonica and O. sativa ssp. indica. The rice sequence data can be used to study the origin of genes and gene families, track rates of sequence divergence over time, and provide hints about how genes evolve and generate products with novel biological properties. The rice sequence data has already been mined to show that transposable elements often carry fragments of cellular genes. This type of genome shuffling could play a role in creating novel, reorganized genes with new adaptive properties.     

Population Size Affects Adaptation in Complex Ways: Simulations on Empirical Adaptive Landscapes

Do large populations always outcompete smaller ones? Does increasing the mutation rate have a similar effect to increasing the population size, with respect to the adaptation of a population? How important are substitutions in determining the adaptation rate? In this study, we ask how population size and mutation rate interact to affect adaptation on empirical adaptive landscapes. Using such landscapes, we do not need to make many ad hoc assumption about landscape topography, such as about epistatic interactions among mutations or about the distribution of fitness effects. Moreover, we have a better understanding of all the mutations that occur in a population and their effects on the average fitness of the population than we can know in experimental studies. Our results show that the evolutionary dynamics of a population cannot be fully explained by the population mutation rate \(N\mu\); even at constant \(N\mu\), there can be dramatic differences in the adaptation of populations of different sizes. Moreover, the substitution rate of mutations is not always equivalent to the adaptation rate, because we observed populations adapting to high adaptive peaks without fixing any mutations. Finally, in contrast to some theoretical predictions, even on the most rugged landscapes we study, small population size is never an advantage over larger population size. These result show that complex interactions among multiple factors can affect the evolutionary dynamics of populations, and simple models should be taken with caution.