Speciation genomics in Ficedula flycatchers

Abstract: Understanding what evolutionary processes have shaped patterns of genomic differentiation between species is a major aim of speciation genomics. However, disentangling the role of different processes that generate similar patterns remains a substantial challenge. Within this thesis, I aimed to infer the action of different evolutionary processes through population-level genome re-sequencing of closely related species. I explored how processes such as recombination, natural selection, and genetic drift interact to shape the genomic differentiation landscape among multiple species of Ficedula flycatcher. Collared flycatcher and pied flycatcher are a pair of closely related species, which hybridize in regions of secondary contact. Reproductive isolation is strong and hybrids appear to be sterile. I compared the differentiation landscape between collared and pied flycatchers with a more distantly related species pair, the red-breasted and taiga flycatchers. This comparison revealed elevated regions of genomic differentiation shared between the two pairs, i.e. shared differentiation peaks, and those unique to a single pair, i.e. lineage-specific differentiation peaks. Since the two species pairs share a negligible portion of genetic variation, shared patterns in the differentiation landscape should be driven and maintained by conserved processes, while lineage-specific patterns should be driven by lineage-specific changes in relevant evolutionary processes. Selective sweep scans suggested that both shared and lineage-specific peaks can result from adaptive evolution and that lineage-specific adaptation is not a sufficient determinant of lineage-specific peaks. Instead, lineage-specific differentiation peaks appeared to be driven by evolutionary changes in the recombination landscape, the dynamics of which had strong impacts on the detection of signatures of linked selection. I also found that adaptation did not play a prominent role on Z-chromosome differentiation. Both the fast-Z and large-Z effects were apparent within the flycatchers but appeared to be primarily driven by the increased role of genetic drift on the Z-chromosome due to its reduced effective population size compared to the autosomes. I hypothesized that the increased impact of genetic drift could speed up the buildup of genetic incompatibilities of Z-linked and autosomal loci and contribute to reproductive isolation. Finally, using long-read and HiC sequencing data, I generated high-quality reference genomes for the collared flycatcher and pied flycatcher, and provided a first glimpse of the role of structural variation in speciation. I observed an increased prevalence of inversions and translocations on the sex chromosomes and in differentiation peaks. Structural rearrangements may therefore represent an important source of genomic variation contributing to species divergence.