Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

Long-term adaptation of epistatic genetic networks

Gene networks are likely to govern most traits in nature. Mutations at these genes often show functional epistatic interactions that lead to complex genetic architectures and variable fitness effects in different genetic backgrounds. Understanding how epistatic genetic systems evolve in nature remains one of the great challenges in evolutionary biology. Here we combine an analytical framework with individual-based simulations to generate novel predictions about long-term adaptation of epistatic networks. We find that relative to traits governed by independently evolving genes, adaptation with epistatic gene networks is often characterized by longer waiting times to selective sweeps, lower standing genetic variation, and larger fitness effects of adaptive mutations. This may cause epistatic networks to either adapt more slowly or more quickly relative to a nonepistatic system. Interestingly, epistatic networks may adapt faster even when epistatic effects of mutations are on average deleterious. Further, we study the evolution of epistatic properties of adaptive mutations in gene networks. Our results show that adaptive mutations with small fitness effects typically evolve positive synergistic interactions, whereas adaptive mutations with large fitness effects evolve positive synergistic and negative antagonistic interactions at approximately equal frequencies. These results provide testable predictions for adaptation of traits governed by epistatic networks and the evolution of epistasis within networks.     

Coalescent under the evolution of coadaptation

Adaptation to novel environments arises either from new beneficial mutations or by utilizing pre‐existing genetic variation. When standing variation is used as the source of new adaptation, fitness effects of alleles may be altered through an environmental change. Alternatively, changes in epistatic genetic backgrounds may convert formerly neutral mutations into beneficial alleles in the new genetic background. By extending the coalescent theory to describe the genealogical histories of two interacting loci, I here investigated the hitchhiking effect of epistatic selection on the amount and pattern of sequence diversity at the linked neutral regions. Assuming a specific form of epistasis between two new mutations that are independently neutral, but together form a coadapted haplotype, I demonstrate that the footprints of epistatic selection differ markedly between the interacting loci depending on the order and relative timing of the two mutational events, even though both mutations are equally essential for the formation of an adaptive gene combination. Our results imply that even when neutrality tests could detect just a single instance of adaptive substitution, there may, in fact, be numerous other hidden mutations that are left undetected, but still play indispensable roles in the evolution of a new adaptation. We expect that the integration of the coalescent framework into the general theory of polygenic inheritance would clarify the connection between factors driving phenotypic evolution and their consequences on underlying DNA sequence changes, which should further illuminate the evolutionary foundation of coadapted systems.     

植物多倍体中的基因组印记

植物多倍体在自然界中广泛存在,这说明拥有多套遗传物质使得多倍体的适应进化具有优势。新多倍体形成后,一些基因组范围的变化较迅速地发生在多倍体形成开端,另一些在长期进化中发生。由于受到遗传、表观等因素的影响,亲本对于新形成多倍体基因组的贡献不均衡。这种偏向于某个亲本基因组的显性优势,称为基因组印记。植物多倍体中的基因组印记表现为基因组偏向性的序列消除、不均衡基因表达、基因沉默,这些受到基因组合并及DNA甲基化、核仁显性等表观因素影响。本文旨在为多倍体基因组进化及育种的相关研究提供参考。     

Evolution of coadaptation in a two-locus epistatic system

Although recent advances in genome biology have dramatically increased our understanding of the contribution of gene interactions to the development of complex phenotypes, we still lack general agreement on the process and mechanisms responsible for the evolution of epistatic systems. Even if genes in a species are indeed integrated into coadapted complexes of interacting components, simple additive evolution may eventually result in epistatic differentiation of populations. Consequently, the prevalence of epistatic gene action does not tell us anything about the role of epistatic selection in the history of population divergence. To elucidate the contribution of epistatic selection in the evolution of coadaptation, we investigate the fixation process of two mutations that interact synergistically to enhance fitness. We show by diffusion analysis and simulations that epistatic selection on cosegregating variants does not by itself promote the evolution of epistatic systems; rather, accumulation of neutral mutations may play a crucial role, creating an appropriate genetic milieu for adaptive evolution in the future generations.     

Testing eco-evolutionary predictions using fossil data: Phyletic evolution following ecological opportunity*

Fossil sequences provide observations of phenotypes within a lineage over time and represent essential data for increasing our understanding of phyletic evolution beyond microevolutionary timescales. I investigate if fossil time series of the diatom Stephanodiscus niagarae/yellowstonensis follow evolutionary dynamics compatible with hypotheses for how the adaptive landscape changes when a population enters a new environment. The lineage—which has a remarkably detailed stratigraphic record—invaded Yellowstone Lake immediately after recession of ice from the basin 14,000 years ago. Several phyletic models portraying different types of evolutionary dynamics—both compatible and not compatible with changes in the adaptive landscape following ecological opportunity—were fitted to the fossil times-series of S. niagarae/yellowstonensis. Different models best describe the three analyzed traits. Two of the models (a new model of decelerated evolution and an Ornstein–Uhlenbeck model) capture trait dynamics compatible with an event of ecological opportunity, whereas the third model (random walk) does not. Entering a new environment may accordingly affect trait dynamics for thousands of years, but the effects can vary across phenotypes. However, tests of model adequacy reveal shortcomings in all three models explaining the trait dynamics, suggesting model development is needed to more fully understand the phyletic evolution in S. niagarae/yellowstonensis.     

Molecular Clock of Neutral Mutations in a Fitness-Increasing Evolutionary Process

The molecular clock of neutral mutations, which represents linear mutation fixation over generations, is theoretically explained by genetic drift in fitness-steady evolution or hitchhiking in adaptive evolution. The present study is the first experimental demonstration for the molecular clock of neutral mutations in a fitness-increasing evolutionary process. The dynamics of genome mutation fixation in the thermal adaptive evolution of Escherichia coli were evaluated in a prolonged evolution experiment in duplicated lineages. The cells from the continuously fitness-increasing evolutionary process were subjected to genome sequencing and analyzed at both the population and single-colony levels. Although the dynamics of genome mutation fixation were complicated by the combination of the stochastic appearance of adaptive mutations and clonal interference, the mutation fixation in the population was simply linear over generations. Each genome in the population accumulated 1.6 synonymous and 3.1 non-synonymous neutral mutations, on average, by the spontaneous mutation accumulation rate, while only a single genome in the population occasionally acquired an adaptive mutation. The neutral mutations that preexisted on the single genome hitchhiked on the domination of the adaptive mutation. The successive fixation processes of the 128 mutations demonstrated that hitchhiking and not genetic drift were responsible for the coincidence of the spontaneous mutation accumulation rate in the genome with the fixation rate of neutral mutations in the population. The molecular clock of neutral mutations to the fitness-increasing evolution suggests that the numerous neutral mutations observed in molecular phylogenetic trees may not always have been fixed in fitness-steady evolution but in adaptive evolution.     

Pervasive,yet idiosyncratic,epistatic pleiotropy during adaptation in a behaviourally complex microbe

Understanding how multiple mutations interact to jointly impact multiple ecologically important traits is critical for creating a robust picture of organismal fitness and the process of adaptation. However, this is complicated by both environmental heterogeneity and the complexity of genotype‐to‐phenotype relationships generated by pleiotropy and epistasis. Moreover, little is known about how pleiotropic and epistatic relationships themselves change over evolutionary time. The soil bacterium Myxococcus xanthus employs several distinct social traits across a range of environments. Here, we use an experimental lineage of M. xanthus that evolved a novel form of social motility to address how interactions between epistasis and pleiotropy evolve. Specifically, we test how mutations accumulated during selection on soft agar pleiotropically affect several other social traits (hard agar motility, predation and spore production). Relationships between changes in swarming rate in the selective environment and the four other traits varied greatly over time in both direction and magnitude, both across timescales of the entire evolutionary lineage and individual evolutionary time steps. We also tested how a previously defined epistatic interaction is pleiotropically expressed across these traits. We found that phenotypic effects of this epistatic interaction were highly correlated between soft and hard agar motility, but were uncorrelated between soft agar motility and predation, and inversely correlated between soft agar motility and spore production. Our results show that ‘epistatic pleiotropy’ varied greatly in magnitude, and often even in sign, across traits and over time, highlighting the necessity of simultaneously considering the interacting complexities of pleiotropy and epistasis when studying the process of adaptation.     

Adapting to winter in wheat: a long-term study follows parallel phenotypic and genetic changes in three experimental wheat populations

Drawing a direct connection between adaptive evolution at the phenotypic level and underlying genetic factors has long been a major goal of evolutionary biologists, but the genetic characterization of adaptive traits in natural populations is notoriously difficult. The study of evolution in experimental populations offers some help — initial conditions are known and changes can be tracked for extended periods under conditions more controlled than wild populations and more realistic than laboratory or greenhouse experiments. In this issue of Molecular Ecology , researchers studying experimental wheat populations over a 12-year period have demonstrated evolution in a major adaptive trait, flowering time, and parallel changes in underlying genetic variation ( Rhoné et al . 2008 ). Their work suggests that cis -regulatory mutations at a single gene may explain most of the flowering time variation in these populations.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF INDIRECT GENETIC EFFECTS: CHANGES IN THE INTERACTION EFFECT COEFFICIENT,PSI (Ψ), DUE TO SEXUAL SELECTION

Indirect genetics effects (IGEs)—when the genotype of one individual affects the phenotypic expression of a trait in another—may alter evolutionary trajectories beyond that predicted by standard quantitative genetic theory as a consequence of genotypic evolution of the social environment. For IGEs to occur, the trait of interest must respond to one or more indicator traits in interacting conspecifics. In quantitative genetic models of IGEs, these responses (reaction norms) are termed interaction effect coefficients and are represented by the parameter psi (Ψ). The extent to which Ψ exhibits genetic variation within a population, and may therefore itself evolve, is unknown. Using an experimental evolution approach, we provide evidence for a genetic basis to the phenotypic response caused by IGEs on sexual display traits in Drosophila serrata. We show that evolution of the response is affected by sexual but not natural selection when flies adapt to a novel environment. Our results indicate a further mechanism by which IGEs can alter evolutionary trajectories—the evolution of interaction effects themselves.     

A simple model of co-evolutionary dynamics caused by epistatic selection

Epistasis is the dependency of the effect of a mutation on the genetic background in which it occurs. Epistasis has been widely documented and implicated in the evolution of species barriers and the evolution of genetic architecture. Here we propose a simple model to formalize the idea that epistasis can also lead to co-evolutionary patterns in molecular evolution of interacting genes. This model epistasis is represented by the influence of one gene substitution on the fitness rank of the resident allele at another locus. We assume that increasing or decreasing fitness rank occur equally likely. In simulations we show that this form of epistasis leads to co-evolution in the sense that the length of an adaptive walk between interacting loci is highly correlated. This effect is caused by episodes of elevated rate of evolution in both loci simultaneously. We find that the influence of epistasis on these measures of co-evolutionary dynamics is relatively robust to the details of the model. The main factor influencing the correlation in evolutionary rates is the probability that a substitution will have an epistatic effect, but the strength of epistasis or the asymmetry of the initial fitness ranks of the alleles have only a minor effect. We suggest that covariance in rates of evolution among loci could be used to detect epistasis among loci.     

A test for Y‐linked additive and epistatic effects on surviving bacterial infections in Drosophila melanogaster

Y‐ and W‐chromosomes offer a theoretically powerful way for sexual dimorphism to evolve. Consistent with this possibility, Drosophila melanogaster Y‐chromosomes can influence gene regulation throughout the genome; particularly immune‐related genes. In order for Y‐linked regulatory variation (YRV) to contribute to adaptive evolution it must be comprised of additive genetic variance, such that variable Ys induce consistent phenotypic effects within the local gene pool. We assessed the potential for Y‐chromosomes to adaptively shape gram‐negative and gram‐positive bacterial defence by introgressing Ys across multiple genetic haplotypes from the same population. We found no Y‐linked additive effects on immune phenotypes, suggesting a restricted role for the Y to facilitate dimorphic evolution. We did find, however, a large magnitude Y by background interaction that induced rank order reversals of Y‐effects across the backgrounds (i.e. sign epistasis). Thus, Y‐chromosome effects appeared consistent within backgrounds, but highly variable among backgrounds. This large sign epistatic effect could constrain monomorphic selection in both sexes, considering that autosomal alleles under selection must spend half of their time in a male background where relative fitness values are altered. If the pattern described here is consistent for other traits or within other XY (or ZW) systems, then YRV may represent a universal constraint to autosomal trait evolution.     

The relation between multilocus population genetics and social evolution theory

Evolution at multiple gene positions is complicated. Direct selection on one gene disturbs the evolutionary dynamics of associated genes. Recent years have seen the development of a multilocus methodology for modeling evolution at arbitrary numbers of gene positions with arbitrary dominance and epistatic relations, mode of inheritance, genetic linkage, and recombination. We show that the approach is conceptually analogous to social evolutionary methodology, which focuses on selection acting on associated individuals. In doing so, we (1) make explicit the links between the multilocus methodology and the foundations of social evolution theory, namely, Price's theorem and Hamilton's rule; (2) relate the multilocus approach to levels-of-selection and neighbor-modulated-fitness approaches in social evolution; (3) highlight the equivalence between genetical hitchhiking and kin selection; (4) demonstrate that the multilocus methodology allows for social evolutionary analyses involving coevolution of multiple traits and genetical associations between nonrelatives, including individuals of different species; (5) show that this methodology helps solve problems of dynamic sufficiency in social evolution theory; (6) form links between invasion criteria in multilocus systems and Hamilton's rule of kin selection; (7) illustrate the generality and exactness of Hamilton's rule, which has previously been described as an approximate, heuristic result.     

Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli

The extent and nature of epistatic interactions between mutations are issues of fundamental importance in evolutionary biology. However, they are difficult to study and their influence on adaptation remains poorly understood. Here, we use a systems-level approach to examine epistatic interactions that arose during the evolution of Escherichia coli in a defined environment. We used expression arrays to compare the effect on global patterns of gene expression of deleting a central regulatory gene, crp. Effects were measured in two lineages that had independently evolved for 20,000 generations and in their common ancestor. We found that deleting crp had a much more dramatic effect on the expression profile of the two evolved lines than on the ancestor. Because the sequence of the crp gene was unchanged during evolution, these differences indicate epistatic interactions between crp and mutations at other loci that accumulated during evolution. Moreover, a striking degree of parallelism was observed between the two independently evolved lines; 115 genes that were not crp-dependent in the ancestor became dependent on crp in both evolved lines. An analysis of changes in crp dependence of well-characterized regulons identified a number of regulatory genes as candidates for harboring beneficial mutations that could account for these parallel expression changes. Mutations within three of these genes have previously been found and shown to contribute to fitness. Overall, these findings indicate that epistasis has been important in the adaptive evolution of these lines, and they provide new insight into the types of genetic changes through which epistasis can evolve. More generally, we demonstrate that expression profiles can be profitably used to investigate epistatic interactions.     

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.     

The evolving fungal genome

Fungal genomes vary considerably in size and organization. The genome of Microsporidium contains less than 3 Mb while the genomes of several Basidiomycetes and Ascomycetes greatly exceed 100 Mb. Likewise chromosome numbers and ploidy levels can differ even between closely related species. The differences in genome architecture among fungi reflect the interplay of different mutational processes as well as the population biology of the different species. Comparative genome studies have elucidated the underlying mechanisms of genome evolution in different groups of fungi and have provided insight into species-specific genomic traits. Mobile genetic elements have been instrumental in shaping the genome architecture and gene content in many fungal species. In many pathogenic fungi the mobile genetic elements even play a crucial role in rapid adaptive evolution by mediating high rates of sequence mutations, chromosomal rearrangements, and ploidy changes. But in many species mobile elements are efficiently restricted by defense mechanisms, which have evolved to suppress and regulate parasitic elements. Different rates of genome dynamic and adaptive evolution may reflect varying effective population sizes through which genetic drift and natural selection have differentially affected genome architecture in fungi over time.     

Beyond mean allelic effects: A locus at the major color gene MC1R associates also with differing levels of phenotypic and genetic (co)variance for coloration in barn owls

The mean phenotypic effects of a discovered variant help to predict major aspects of the evolution and inheritance of a phenotype. However, differences in the phenotypic variance associated to distinct genotypes are often overlooked despite being suggestive of processes that largely influence phenotypic evolution, such as interactions between the genotypes with the environment or the genetic background. We present empirical evidence for a mutation at the melanocortin‐1‐receptor gene, a major vertebrate coloration gene, affecting phenotypic variance in the barn owl, Tyto alba. The white MC1R allele, which associates with whiter plumage coloration, also associates with a pronounced phenotypic and additive genetic variance for distinct color traits. Contrarily, the rufous allele, associated with a rufous coloration, relates to a lower phenotypic and additive genetic variance, suggesting that this allele may be epistatic over other color loci. Variance differences between genotypes entailed differences in the strength of phenotypic and genetic associations between color traits, suggesting that differences in variance also alter the level of integration between traits. This study highlights that addressing variance differences of genotypes in wild populations provides interesting new insights into the evolutionary mechanisms and the genetic architecture underlying the phenotype.