Balancing selection: Ecological causes & genetic footprints

The concept of balancing selection refers to ecological and evolutionary mechanisms that can maintain two or more alleles at a locus in a population. Important examples for such mechanisms are heterozygote advantage, selection pressures varying across time and space, differences in the way genotypes compete for resources and respond to competition, and host-parasite interactions. These mechanisms are not necessarily mutually exclusive; for example some of the temporally heterogeneous scenarios cause heterozygotes to have a higher geometric mean fitness than homozygotes. Depending on ecological scenario and genetic architecture, alleles can be regularly regenerated by new mutations (allelic turnover) or stably maintained over extremely long time periods, even across species or genera. Such trans-specific polymorphisms have recently been found in many taxonomic groups, including the fruit fly genus Drosophila and the plant genus Arabidopsis. However, it is currently unclear how to distinguish between the various possible mechanisms of diversity maintenance based on genetic data. In this project, we will combine modeling approaches from evolutionary ecology (adaptive dynamics) and from population genetics (coalescent theory) to derive the expected genetic footprints of balancing selection under spatio-temporal heterogeneity, boom-bust competition scenarios, and host-parasite coevolution mechanisms that have been implicated in diversity maintenance in Drosophila and Arabidopsis. Based on these results, we will develop a classification framework of ecological scenarios, which will highlight the potential and the limitations for inferring mechanisms underlying long-term balancing selection from genetic data. Using this framework, we will then infer or narrow down possible explanations for trans-specific polymorphism in Drosophila and Arabidopsis.

Individuals within a population usually differ from each other in many ways, also genetically. One of the most important questions in evolutionary biology is how this diversity within populations arises and how it is maintained over long periods of time. We want to understand, for example, how much genetic variation is maintained by the various types of balancing selection, for example by heterozygote advantage or temporally fluctuating selection. As one part of the project, we described an additional mechanism for balancing selection for populations with density-dependent growth in a seasonally fluctuating environment.Balancing selection not only maintains diversity at certain sites in the genome but can also influence patterns of genetic variation in neighboring regions of the genome. This is the so- called footprint of selection. To be able to infer the underlying evolutionary process from the genetic footprint we need detailed predictions for the footprints of various processes. An important part of this project was to characterize the genetic footprint to be expected when a genetic polymorphism is maintained by temporally fluctuating environmental conditions. For this, we used computer simulations as well as analytic and numeric computations. Our results show an increased diversity around the polymorphism, as in the case of heterozygote advantage. However, unlike for heterozygote advantage, temporally fluctuating selection also leads to a reduction in diversity further away from the selected site. Based on this difference it is possible in principle to distinguish between the mechanisms in empirical data. However, only under certain conditions (e.g. relatively strong selection) will the expected reduction in diversity be strong enough to be detectable in real data. Nevertheless, such a reduction in diversity can have important evolutionary implications because it affects large parts of the respective chromosome or even the whole genome. If multiple loci are under temporally fluctuating selection they can jointly lead to a strong reduction in genome-wide diversity, which in turn reduces the ability of the population to adapt and cope with a changing environment. Further interesting phenomena arise when multiple loci in close proximity are under fluctuating selection. Depending on the initial conditions we then observe more or less strong coupling between the loci, which leads to either weak or strong genetic footprints. A further aspect explored in this project is the length of the trans-specific haplotype around a polymorphism under selection, i.e. the length of the haplotype that is shared between closely related species. Again, we found differences between the various mechanisms for balancing selection.