The Genetics of Adaptation in Changing Environments

The aim of the proposed project is to study the genetic basis of adaptation to environmental change, using biomathematical modeling and computer simulations. Adaptation is central to Darwinian evo-lution, and it may be a key to the survival of species under the conditions of human-induced global change. Despite its importance, many basic questions about the genetic basis of adaptation are still un-resolved. This is particularly true for adaptation to gradual change, such as the rise of global temperature and atmospheric CO2, or increases in UV radiation and the concentration of pollutants. To understand the consequences of gradual change, it is important to develop theory with increased ecological realism. Recently, several authors (including the PI of the present proposal) have started to investigate models of selection towards a moving optimum, which naturally combine genetic and environmental dynamics. Here, we propose to further develop this theory by employing more complex and realistic genetic assumptions. We wish to better understand how the adaptive process is shaped by the available standing genetic variation and by the properties of the (multidimensional) genotype-to-phenotype-to-fitness map. Throughout, our focus will be not on evolution at the phenotypic level, but on the substitution processes at individual genetic loci (i.e. the number and size of adaptive steps). Developing such theory is timely, because it is needed to interpret the growing amount of data on the genetic basis of adaptation that is becoming available due to the application of modern genomic techniques. We also aim to derive general and testable predictions, which can be evaluated, for example, by microbial evolution experiments. Specifically, we propose two complementary subprojects: First, we will study the distribution of adaptive substitutions (i.e. the distribution of the effects of fixed beneficial mutations) arising from standing genetic variation and compare it to that derived from new mutations. We will also study how the relative importance of these two sources of variation changes over time. In particular, we ask if and when there is a "phase transition" between short- and long-term adaptation. In this subproject, we will not only consider the moving-optimum scenario, but also selection towards a constant optimum and truncation selection. The project will be an important step towards bridging the gap between models of phenotypic and molecular evolution, since standing genetic variation has been treated as ubiquitous in the former but almost completely ignored in the latter. Second, we will study moving-optimum models in high-dimensional trait spaces. As a starting point, we will analyze a model with two genetically correlated traits. Then, we will develop a moving-optimum version of Fisher`s geometric model, which treats evolution in n-dimensional spaces with universal pleiotropy. Finally, we will analyze a moving-optimum model with one focal trait, in which mutations have pleiotropic side- effects on fitness. These studies will provide links to previous quantitative genetics theory as well as to more recent "adaptation models", which focus on the high-dimensionality of phenotype spaces and the genotype-to-phenotype- to-fitness map as key characteristic of adaptation at the organismic level.

Natural populations are constantly faced with changing environments like the change in global temperature or in pH-value that force them to adapt to the new environmental conditions. If they fail to adapt, populations will decline in size and eventually go extinct.The fundamental event during adaptation is the substitution of a previously established gene variant by a beneficial mutation. The statistical description of this process is a key to answer seemingly simple questions such as, how many substitutions typically occur during a bout of adaptation, how large is their effect on the organism, how many mutations have already been present before the environmental change, and do complex organisms adapt less easily than simple ones? Answers to these questions are not only of interest to basic research, but can also find applications in conservation biology.In our study Fishers geometric model with a moving optimum we showed that adaptation critically depends on the mode and speed of environmental change relative to the adaptive potential of the population. In the case of a sudden environmental change, genetic adaptation proceeds by many small steps and just a few substitutions of large effect. Adaptation in a constantly changing environment, in contrast, is characterized by many intermediate-sized substitutions. Complex organisms adapt more slowly than simple ones, but they do so in larger steps. Mutations that have been previously present in the population are most important if the environmental change is large and sudden.In a second study (Rapid adaptation of quantitative traits: theoretical perspectives) we summarized the theoretical literature on the scope and limits of genetic adaptation of natural populations to global climate change. In addition, we commented on the question whether empirically observed adaptations can be used to identify endangered populations. We show that, on the one hand, previous criticisms of relevant theoretical models are unjustified, but on the other hand, currently available data lack the precision required for robust predictions.