Population genomics of contemporary evolution in space and time

The capacity of natural populations to evolve in the face of changing environments depends on the dynamics of adaptive (such as natural selection) and neutral processes (such as random genetic drift and migration). Disentangling these processes may help our understanding of evolution and can be used to model and predict future responses to environ­mental changes. In the past, research mainly focused on documenting the rates at which traits evolve. With progress in DNA sequencing technologies, it is now possible to determine the geno­mic under­pinnings of the populations’ evolutionary responses to environmental changes.

The purpose of this research was to determine the genomic basis of rapid evolution of popula­tions of three distinct species: two co-existing stickleback populations in a spatially heteroge­neous environment, and a Daphnia magna water flea population sampled through time by “resurrecting” dormant propagules buried in pond sediments. In addition, I developed geno­mic resources for both the stickleback and Daphnia system. This thesis provides answers to the following five broad issues in the field of evolutionary biology. 1) The quantification of the number of genomic regions that respond to selection, i.e. to assess to what extent evolu­tionary responses involve few regions of major effect or many regions of small effect across model organisms. 2) The assessment whether selection occurred via repeated use of same genomic regions (parallel evolution) across species in response to selection along an environ­mental gradient. 3) The assessment of the source of adaptive genetic variation in relation to de novo mutation, gene flow and standing genetic variation. 4) The quantification of the degree of reversibility of alleles due to relaxation in selection pressure. 5) The development of genomic resources to support adaptation research in stickleback and Daphnia.

The study of phenotypes and genotypes revealed that two stickleback species respond to the same environmental challenges in a parallel manner phenotypically while in a non-parallel manner at the genomic level. These responses are also dependent on demography and the life history of the species. In the case of small populations with a better capability of migra­tion, gene flow helps with the recycling of those alleles into the system, which are beneficial for longer term persistence and evolution of populations. Resurrection genomics of D. magna suggests that populations with large effective population sizes (Ne) can withstand strong selection pres­su­res such as predation. The large Ne also enhances effective recombination, which facilitates the distribution of adaptive genomic variation among individuals. Hence, the popu­la­tion has again achieved a larger capacity to rapidly adapt, based solely on standing genetic variation. Altogether, the spatial and temporal population studies of vertebrate and inverte­brate species reveal a large number of genomic islands of differentiation, suggesting a polygenic nature of adaptation. My research also sheds light on the importance of regulatory elements such as micro-RNAs (miRNA) in adaptation research. In conclusion, my research suggests a highly versatile and multifaceted genomic basis of adaptation.