Dynamiques éco-évolutives en populations asexuées : sauvetage évolutif dans le paysage adaptatif de Fisher

The persistence ability of a population facing a stressing environmental change is a complex question at the connection between ecology and evolution. The process by which a population avoid extinction by adapting to the new stressing environmental conditions is termed evolutionary rescue. This particular case of eco-evolutionary dynamic is increasingly investigated both theoretically and experimentally, among other things in the context of the environmental changes from human activity. However, the studies modelling this process neglect the interactions between genotypes and environments impacting the evolutionary potential of the populations facing environmental changes. In the context of this thesis, I developed models integrating these interactions. To this end, I modelled the process of evolutionary rescue in asexual populations, facing abrupt environmental changes, using the adaptive landscape of Fisher (Fisher’s geometric model (1930)). This landscape allowed us to model the genotypes-environments interactions and their impact on the proportion of mutations able to save a population. Using two models, considering either the rescue of a population by a mutation of strong effect, either by a large number of mutation of small effect, we derived predictions for the probability of evolutionary rescue, which depends on the environmental conditions and the characteristics of the studied organism. These models can be parametrized on data from evolutionary experiments and their predictions compared to data of antibiotic treatments aiming on asexual pathogens. Beyond evolutionary rescue, the models developed in this thesis also gave tools to model other eco-evolutionary dynamics, integrating genotype-environment interactions and their effects on the distribution of mutations effects.La capacité de persistance d’une population face à un changement environnemental stressant est une question complexe à l’interface entre l’écologie et l’évolution. Le processus par lequel une population échappe à l’extinction en s’adaptant aux nouvelles conditions environnementales stressantes est nommé sauvetage évolutif. Ce cas particulier de dynamique éco-évolutive est de plus en plus étudié autant théoriquement, qu’expérimentalement, entre autres dans le contexte des changements environnementaux d’origines anthropiques. Cependant, les études modélisant ce processus négligent les interactions entre génotypes et environnements impactant le potentiel évolutif des populations faisant aux changements environnementaux. Dans le cadre de cette thèse, j’ai développé des modèles intégrant ces interactions. Pour cela, j’ai modélisé le processus de sauvetage évolutif de populations à reproduction asexuée, face à des changements environnementaux abruptes, en utilisant le paysage adaptatif de Fisher (modèle géométrique de Fisher (1930)). Ce paysage nous a permis de modéliser ces interactions génotypes-environnement et leur impact sur la proportion de mutations pouvant sauver une population. A travers deux modèles, considérant soit le sauvetage d’une population par une mutation d’effet fort, soit par un grand nombre de mutations d’effets faibles, nous avons pu dégager des prédictions pour la probabilité de sauvetage évolutif en fonction des conditions environnementales et des caractéristiques de l’organisme étudié. Ces modèles peuvent être paramétrés sur des données d’évolution expérimentale et leurs prédictions comparées à des données de traitement antibiotiques visant des pathogènes asexués. Au-delà du sauvetage évolutif, les modèles développés nous ont également permis d’établir des outils permettant de modéliser d’autres dynamiques éco-évolutives, intégrant des interactions génotype-environnement et leurs effets sur la distribution d’effets des mutations

Eco-evolutionary dynamics in asexual populations : evolutionary rescue in Fisher's adaptive landscape

La capacité de persistance d’une population face à un changement environnemental stressant est une question complexe à l’interface entre l’écologie et l’évolution. Le processus par lequel une population échappe à l’extinction en s’adaptant aux nouvelles conditions environnementales stressantes est nommé sauvetage évolutif. Ce cas particulier de dynamique éco-évolutive est de plus en plus étudié autant théoriquement, qu’expérimentalement, entre autres dans le contexte des changements environnementaux d’origines anthropiques. Cependant, les études modélisant ce processus négligent les interactions entre génotypes et environnements impactant le potentiel évolutif des populations faisant aux changements environnementaux. Dans le cadre de cette thèse, j’ai développé des modèles intégrant ces interactions. Pour cela, j’ai modélisé le processus de sauvetage évolutif de populations à reproduction asexuée, face à des changements environnementaux abruptes, en utilisant le paysage adaptatif de Fisher (modèle géométrique de Fisher (1930)). Ce paysage nous a permis de modéliser ces interactions génotypes-environnement et leur impact sur la proportion de mutations pouvant sauver une population. A travers deux modèles, considérant soit le sauvetage d’une population par une mutation d’effet fort, soit par un grand nombre de mutations d’effets faibles, nous avons pu dégager des prédictions pour la probabilité de sauvetage évolutif en fonction des conditions environnementales et des caractéristiques de l’organisme étudié. Ces modèles peuvent être paramétrés sur des données d’évolution expérimentale et leurs prédictions comparées à des données de traitement antibiotiques visant des pathogènes asexués. Au-delà du sauvetage évolutif, les modèles développés nous ont également permis d’établir des outils permettant de modéliser d’autres dynamiques éco-évolutives, intégrant des interactions génotype-environnement et leurs effets sur la distribution d’effets des mutations.The persistence ability of a population facing a stressing environmental change is a complex question at the connection between ecology and evolution. The process by which a population avoid extinction by adapting to the new stressing environmental conditions is termed evolutionary rescue. This particular case of eco-evolutionary dynamic is increasingly investigated both theoretically and experimentally, among other things in the context of the environmental changes from human activity. However, the studies modelling this process neglect the interactions between genotypes and environments impacting the evolutionary potential of the populations facing environmental changes. In the context of this thesis, I developed models integrating these interactions. To this end, I modelled the process of evolutionary rescue in asexual populations, facing abrupt environmental changes, using the adaptive landscape of Fisher (Fisher’s geometric model (1930)). This landscape allowed us to model the genotypes-environments interactions and their impact on the proportion of mutations able to save a population. Using two models, considering either the rescue of a population by a mutation of strong effect, either by a large number of mutation of small effect, we derived predictions for the probability of evolutionary rescue, which depends on the environmental conditions and the characteristics of the studied organism. These models can be parametrized on data from evolutionary experiments and their predictions compared to data of antibiotic treatments aiming on asexual pathogens. Beyond evolutionary rescue, the models developed in this thesis also gave tools to model other eco-evolutionary dynamics, integrating genotype-environment interactions and their effects on the distribution of mutations effects

When sinks become sources: adaptive colonization in asexuals

The successful establishment of a population into a new empty habitat outside of its initial niche is a phenomenon akin to evolutionary rescue in the presence of immigration. It underlies a wide range of processes, such as biological invasions by alien organisms, host shifts in pathogens or the emergence of resistance to pesticides or antibiotics from untreated areas.[br/] In this study, we derive an analytically tractable framework to describe the coupled evolutionary and demographic dynamics of asexual populations in a source-sink system. In particular, we analyze the influence of several factors — immigration rate, mutational parameters, and harshness of the stress induced by the change of environment — on the establishment success in the sink (i.e. the formation of a self-sufficient population in the sink), and on the time until establishment. To this aim, we use a classic phenotype-fitness landscape (Fisher’s geometrical model in n dimensions) where source and sink habitats determine distinct phenotypic optima. The harshness of stress, in the sink, is determined by the distance between the fitness optimum in the sink and that of the source. The dynamics of the full distribution of fitness and of population size in the sink are analytically predicted under a strong mutation strong immigration limit where the population is always polymorphic.[br/] The resulting eco-evolutionary dynamics depend on mutation and immigration rates in a non straightforward way. Below some mutation rate threshold, establishment always occurs in the sink, following a typical four-phases trajectory of the mean fitness. The waiting time to this establishment is independent of the immigration rate and decreases with the mutation rate. Beyond the mutation rate threshold, lethal mutagenesis impedes establishment and the sink population remains so, albeit with an equilibrium state that depends on the details of the fitness landscape. We use these results to get some insight into possible effects of several management strategies

Evolutionary Rescue over a Fitness Landscape

International audienceEvolutionary rescue describes a situation where adaptive evolution prevents the extinction of a population facing a stressing environment. Models of evolutionary rescue could in principle be used to predict the level of stress beyond which extinction becomes likely for species of conservation concern, or, conversely, the treatment levels most likely to limit the emergence of resistant pests or pathogens. Stress levels are known to affect both the rate of population decline (demographic effect) and the speed of adaptation (evolutionary effect), but the latter aspect has received less attention. Here, we address this issue using Fisher's geometric model of adaptation. In this model, the fitness effects of mutations depend both on the genotype and the environment in which they arise. In particular, the model introduces a dependence between the level of stress, the proportion of rescue mutants, and their costs before the onset of stress. We obtain analytic results under a strong-selection-weak-mutation regime, which we compare to simulations. We show that the effect of the environment on evolutionary rescue can be summarized into a single composite parameter quantifying the effective stress level, which is amenable to empirical measurement. We describe a narrow characteristic stress window over which the rescue probability drops from very likely to very unlikely as the level of stress increases. This drop is sharper than in previous models, as a result of the decreasing proportion of stress-resistant mutations as stress increases. We discuss how to test these predictions with rescue experiments across gradients of stress

Supplementary file 2

Supplementary file 2 provides the Matlab© (MATLAB 2015a, The MathWorks, Natick, 2015) source code for the curve fitting procedure used for Eq.[8]

Supplementary file 1

Supplementary file 1 provides the details of the analytical derivations, the code producing the figures and the simulation code as a Mathematica© .cdf file (MATHEMATICA v. 11.3 Wolfram Research 2018) which can be open using the free “CDF player” available on the Wolfram websit

Population persistence under high mutation rate: from evolutionary 1 rescue to lethal mutagenesis

International audiencePopulations may genetically adapt to severe stress that would otherwise cause their extirpation. Recent theoretical work, com-bining stochastic demography with Fisher’s geometric model of adaptation, has shown how evolutionary rescue becomes unlikelybeyond some critical intensity of stress. Increasing mutation rates may however allow adaptation to more intense stress, raisingconcerns about the effectiveness of treatments against pathogens. This previous work assumes that populations are rescued bythe rise of a single resistance mutation. However, even in asexual organisms, rescue can also stem from the accumulation ofmultiple mutations in a single genome. Here, we extend previous work to study the rescue process in an asexual population wherethe mutation rate is sufficiently high so that such events may be common. We predict both the ultimate extinction probability ofthe population and the distribution of extinction times. We compare the accuracy of different approximations covering a largerange of mutation rates. Moderate increase in mutation rates favors evolutionary rescue. However, larger increase leads to extinc-tion by the accumulation of a large mutation load, a process called lethal mutagenesis. We discuss how these results could helpdesign “evolution-proof” antipathogen treatments that even highly mutable strains could not overcome

Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence.

Speciation results from the progressive accumulation of mutations that decrease the probability of mating between parental populations or reduce the fitness of hybrids-the so-called species barriers. The speciation genomic literature, however, is mainly a collection of case studies, each with its own approach and specificities, such that a global view of the gradual process of evolution from one to two species is currently lacking. Of primary importance is the prevalence of gene flow between diverging entities, which is central in most species concepts and has been widely discussed in recent years. Here, we explore the continuum of speciation thanks to a comparative analysis of genomic data from 61 pairs of populations/species of animals with variable levels of divergence. Gene flow between diverging gene pools is assessed under an approximate Bayesian computation (ABC) framework. We show that the intermediate "grey zone" of speciation, in which taxonomy is often controversial, spans from 0.5% to 2% of net synonymous divergence, irrespective of species life history traits or ecology. Thanks to appropriate modeling of among-locus variation in genetic drift and introgression rate, we clarify the status of the majority of ambiguous cases and uncover a number of cryptic species. Our analysis also reveals the high incidence in animals of semi-isolated species (when some but not all loci are affected by barriers to gene flow) and highlights the intrinsic difficulty, both statistical and conceptual, of delineating species in the grey zone of speciation

Supplemental Material for Anciaux et al., 2018

<b>File S1</b> contains appendices describing all analytical derivations and supplementary figures. <b>File S2</b> provides the details of the analytical derivations as a Mathematica^© source code (<i>MATHEMATICA v. 9.0 </i>Wolfram Research 2012). <b>File S3 </b>provides the simulation code also as a Mathematica^© source code (<i>MATHEMATICA v. 9.0 </i>Wolfram Research 2012)