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Guillaume Martin
Institut des Sciences de l'Evolution, UMR 5554

Can we predict adaptation trajectories on simple fitness landscapes?


Author(s): Martin, G


The dynamics of adaptation to a new environment is inherently complex, even in the simplest situations such as encountered in experimental evolution). Over the past decades, several empirical studies have measured the long-term dynamics of adaptation in different model species (mostly micro-organisms). Yet, existing theory does not, to our knowledge, provide quantitative predictions to which such trajectories could be compared. Indeed, the speed with which a population adapts (i.e. the speed of the mean fitness increase) depends on the rate, fitness effects, and fate of beneficial mutations. While tremendous progress has been made in modelling these processes in steady state regimes, the key parameters are still difficult to measure, and more important, they vary over time in observed adaptive trajectories, because of background dependence effects (epistasis). The net result is that populations do not simply adapt linearly over time (i.e. at some steady state rate of increase), and the form of this non-linearity is not predicted by any widely accepted model. Our goal here will be to show that some tools exist that provide testable predictions in this context, and check on a few examples if these predictions are accurate. We will first present some old and new results on Fisher’s model and how they allow to predict the change in rate and effect of beneficial mutations over adaptive trajectories, from empirically measurable deleterious mutation effects and rate. Then we will discuss several alternative tools that can be used to model adaptation trajectories in these types of landscapes, accounting for non - stationary distributions of mutation effects and rates. We will illustrate the use of this approach on some empirical trajectories in model species.

Tim Cooper
University of Houston
Department of Biology and Biochemistry
United States

Epistasis and evolvability in experimentally evolved populations of Escherichia coli


Author(s): Cooper, TF


Epistatic interactions between mutations play a prominent role in many evolutionary theories. Many studies have found that epistasis is widespread, but direct analyses of epistasis can be technically difficult and has not generally considered beneficial mutations. We analyse the effects of epistasis on fitness in a set of genotypes including all combinations of the first five beneficial mutations to fix in an experimental population of Escherichia coli. We show that epistasis depends strongly on the fitness effects of the combined mutations – the larger the expected benefit, the more negative the effect of epistasis on fitness. A similar pattern of interactions is also seen among a set of seven mutations that substituted in a population that was selected in an environment containing a combination of two sugars. Epistasis thus tended to follow a simple relationship of diminishing returns with genotype fitness. This observation supports a model that predicts negative epistasis explains a decelerating rate of adaptation as populations approach a fitness peak. Preliminary experiments are consistent with this prediction, finding that the effective size, but not rate, of beneficial mutations declines across a series of replay populations started from genotypes of progressively higher fitness.

Joachim Krug
University of Cologne
Institute for Theoretical Physics

Epistatic constraints and evolutionary predictability on empirical fitness landscapes


Author(s): Krug, J


The adaptive dynamics of an asexual population in the space of genotypes is constrained by epistatic interactions between mutations at different genetic loci. Recent empirical studies have shown that this strongly reduces the number of mutational pathways that are accessible under conditions of strong selection and weak mutation (SSWM). In the talk I will describe statistical models for fitness landscapes that quantify evolutionary accessibility under different assumptions on the amount of epistasis as well as on the underlying genetic architecture, and show how these models can be used to classify and interpret empirical data sets. I then discuss the impact of epistatic constraints on the predictability of evolutionary trajectories in asexuals, with particular emphasis on the role of population size. With increasing population size clonal interference implies a preference for mutational steps of large effect, which leads to an increase in predictability beyond the expectation under SSWM dynamics. However, a further increase of population size reduces predictability by opening up new pathways that involve the crossing of fitness valleys by multiple mutations. This nonmonotonic pattern of evolutionary predictability is found in large-scale simulations on an empirical fitness landscape, and argued to be observable in experiments that monitor the variability of fitness trajectories among replicate populations.

Alison Duncan
Universite of Montpellier 2

Experimental host-parasite coevolution in temporally variable environments


Author(s): Duncan, AB, Jacob, F, Dusi, E, Hochberg, M, Kaltz, O


Antagonistic, host-parasite coevolution is predicted to be an important driver of genetic change. Despite this, few examples exist from natural populations, possibly because temporal environmental variation may interfere with the co-evolutionary process.

Here we investigate experimental co-evolution between Pseudomonas fluorescens and its phage SBW2Φ2 in a fluctuating temperature environment, changing between permissive (28ºC) and restrictive (32ºC) conditions, for phage populations. We investigated how the frequency of environmental change influenced coevolution in populations experiencing temperature switches every 2, 4 or 8 days, over a 16-day period. Phage persistence is severely reduced at 32ºC, thus we hypothesised that longer periods at 32ºC would be detrimental for the phage.

We found that coevolutionary dynamics under fine-grained fluctuations (every 2 or 4 days) did not differ from the constant 28ºC control. Contrary to expectation, coarse-grained fluctuations (every 8 days) benefited phage populations, despite extended periods at 32ºC. During periods of 32ºC, bacteria flourished in an environment where phage were unable to infect, but also lost previously acquired resistance. Although infections did not occur at 32ºC, all phage populations persisted. Accordingly, once populations were returned to 28ºC, phage benefitted from high infection rates of susceptible bacteria. Our results highlight the need to consider temporal environmental heterogeneity when investigating coevolutionary interactions.

Jasmine Ono
University of British Columbia
Department of Zoology

Genetic interactions between beneficial mutations in Saccharomyces cerevisiae


Author(s): Ono, J, Gerstein, AC, Otto, SP


Independently evolving populations may adapt to similar selection pressures via different genetic changes. The interactions between such changes can then inform us about the underlying fitness landscape, allowing us to determine whether gene flow would be facilitated or hampered following secondary contact. We used Saccharomyces cerevisiae to measure the genetic interactions between independently evolved first-step mutations to the fungicide nystatin. We found that genetic interactions are prevalent, even among the first adaptive mutations. In the adaptive environment, the more beneficial mutation often masks the other, less beneficial one. This would allow a population fixed for the less beneficial allele to acquire and fix a more beneficial allele - thus continuing to climb the adaptive peak. In one case, however, reciprocal sign epistasis was observed, indicative of a fitness valley between two peaks. This is surprising given the small number of mutations combined and the relative simplicity of the adaptive environment.

Daniel Goldhill
Yale University
Ecology and Evolutionary Biology
United States

Genetic robustness and environmental robustness in an RNA virus


Author(s): Goldhill, D, Turner, PE


Robustness, the ability of phenotypes to withstand perturbation, is often categorized into environmental robustness, resistance to environmental change, and genetic robustness, resistance to mutation. Determining how robustness interacts with the fitness landscape is vital to increasing our understanding of how organisms successfully adapt to changing environments. Studies in proteins and RNA molecules have shown that areas of the fitness landscape with high environmental robustness have high genetic robustness, a property that has been termed plastogenetic congruence. However, it is unknown how environmental and genetic robustness relate at higher levels of biological organization such as organisms. We have experimentally evolved an RNA virus, ϕ6, to have higher resistance to heat shock, a form of environmental robustness. We have tested the virus for genetic robustness using a mutagen and shown that the evolved virus maintained higher fitness and therefore had higher genetic robustness. Previous work with this virus has shown that increased genetic robustness does not necessarily lead to increased environmental robustness. Our investigations of the mutations leading to increased robustness allow us to suggest a mechanism linking environmental and genetic robustness in an RNA virus. The study of robustness at the level of a virus provides insight into the nature of the fitness landscape and may help predict evolutionary trajectories.

Lilia Perfeito
Instituto Gulbenkian de Ciência

Impact of gene architecture on the adaptation rate


Author(s): Perfeito, L, Godinho Ferreira, M


The accumulation of spontaneous beneficial mutations is one of the drivers of survival and adaptation in novel environments. Predicting the fitness effects of mutations and explaining them from a functional point of view are among the major goals of modern evolutionary biology. The rate and effects of spontaneous beneficial mutations are expected to depend on the environment, on demography and on genotype. Different models have been proposed to predict and explain the effects of new mutations from the underlying phenotypes. Here we measure the adaptation rate of fission yeast strains with different genome architectures. These strains have identical gene composition. However, they vary in gene expression and show substantial variation for fitness. By following the course of evolution of neutral markers in populations of these strains, we are able to estimate the rate and distribution of effects of new mutations. We use a variant of Fisher's geometrical model (FGM) which can explain the data, while capturing the functional details of the system. FGM predicts that the adaptation rate is a function of initial fitness, even when these differences come from changes affecting multiple genes, as is the case with genomic rearrangements. Our results, taken together with recent observations in experimental evolution, point to the existence of a single peaked landscape with minute complexities at the microscopy level, but a smooth upward climb on the macroscopic level.

Anita Melnyk
Faculty of Science at the University of Ottawa
Department of Biology

Landscape ruggedness reduces genomic parallelism in experimental populations of Pseudomonas


Author(s): Melnyk, AH, Kassen, R


The repeatability of adaptive evolution depends on the ruggedness of the underlying adaptive landscape, how fitness varies as a function of phenotype or genotype. Rugged landscapes are thought to promote divergent adaptation, with genotypes evolving towards distinct genotypic and phenotypic solutions determined by the number of available fitness peaks. By contrast, genotypes evolving on a smooth landscape containing a single adaptive peak are expected to converge on a single genotypic and phenotypic solution. Here we evaluate the genomic consequences of adaptation on rugged and smooth landscapes by quantifying the degree of genic parallelism observed following adaptive evolution by genetically distinct starting genotypes of Pseudomonas fluorescens evolving on two single carbon substrates, xylose and glucose. Previous work showed that these substrates differ in the number of adaptive solutions available to these genotypes, with xylose being a relatively more rugged landscape than glucose. We find that, consistent with expectation, DNA sequence evolution is less parallel in a rugged, compared to a smooth landscape. Our results suggest that the ruggedness of the adaptive landscape has a strong influence on the pattern of genomic evolution.

Nichola Hawkins
Rothamsted Research
Biological Chemistry and Crop Protection
United Kingdom

Mapping the adaptive landscape of Mycosphaerella graminicola CYP51 under selection by azole fungicides


Author(s): Hawkins, NJ, Cools, HJ, Fraaije, BA


The evolution of resistance to drugs and pesticides is a prime example of evolution in action. In many cases, such as the evolution of resistance to QoI and MBC fungicides in fungal pathogens of plants, the adaptive landscape is very simple, with a single mutation effectively conferring full resistance. However, in the case of the azole fungicides, multiple mutations in the target-site-encoding gene CYP51 occur in various combinations, with quantitative and epistatic effects on fungicide sensitivity and enzyme function. Epistatic interactions between mutations may result in rugged fitness landscapes, and incomplete cross-resistance between azoles causes the fitness landscape to shift as different fungicides are used. Mycosphaerella graminicola (Mycosphaerellaceae, Ascomycota) is a major foliar pathogen of wheat, causing yield losses of up to 50%. Azoles have been used extensively to control M. graminicola, but many CYP51 mutations have been reported, with up to eight coding changes in one haplotype, reducing the effectiveness of some compounds. Tools available to investigate M. graminicola CYP51 mutations include functional studies through heterologous expression and homologous gene replacement, experimental evolution through UV mutagenesis and in vitro selection, and historical studies with 160 years of archived samples from Rothamsted's Broadbalk long-term winter wheat field experiment. We consider the value of modelling the evolution of M. graminicola CYP51 as an adaptive landscape, both in formulating anti-resistance strategies for azole use in agriculture, and in addressing fundamental evolutionary questions such as historical contingency and the crossing of adaptive valleys.

Josianne Lachapelle
University of Edinburgh
Institute of Evolutionary Biology
United Kingdom

Selection in different levels of stress and its effects on fitness across a gradient of environmental conditions


Author(s): Lachapelle, J, Colegrave, N


Most environments are variable over time or space, and the populations that are still surviving today have therefore most likely experienced many different environmental conditions. The performance of a population in a novel environment is likely to depend on its own particular selection history if the amplitude and direction of the correlation between the fitness landscapes of the past and novel environments is highly variable along a gradient of environmental conditions. We tested the prediction that adaptation to an intermediate level of stress would enhance performance across a gradient of permissive to stressful conditions by running a selection experiment in the unicellular alga Chlamydomonas reinhardtii. We selected replicated populations for about 40 generations in different levels of stress along an environmental gradient, and then measured their performance in their own as well as in all other levels of stress. We carried the experiment in six different environmental gradients and using three different strains to determine if the particular fitness landscape of the environment and/or the genetic architecture of the strain have an effect on the universality of the results. The results of this experiment will contribute in increasing our understanding of the effects of selection history on performance across a range of possible future environmental conditions.


Chairman: Octávio S. Paulo
Tel: 00 351 217500614 direct
Tel: 00 351 217500000 ext22359
Fax: 00 351 217500028


XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon


Computational Biology & Population Genomics Group