Exploring the genetic basis of migratory traits in Phylloscopus warblers

Each year as the seasons turn, the skies fill with millions of travellers. From the tundra to the tropics, birds embark on remarkable journeys guided by an innate programme and perform one of nature’s most remarkable phenomena: migration. In this thesis, I tackle the study of the genetic basis of migratory behaviour in several Phylloscopus species with a multimodal approach. Here, I combine geolocator data (Papers II, V and VI) with molecular analyses (Papers I, II, IV, V and VI), cytogenetics (Paper IV) and genomic exploration (Papers I, IV and V) in order to identify and dissect genomic regions that may influence the migratory phenotype. In Paper I, we described a repeat-rich region (named MARB) that segregates across two migratory phenotypes of willow warblers P. trochilus with a high density of transposable elements (TEs) and other repetitive sequences. We developed a qPCR-based protocol that enabled us to genotype birds in further studies. In Paper II, we tracked 72 willow warblers throughout Sweden overlapping the hybrid zone, and genotyped them using the protocol from Paper I. We then studied the correlation between the migratory route (phenotype) and divergent genomic regions (genotype) in the willow warbler genome. In Paper III, we reviewed the current state of the field and provided hypotheses for the genetic basis of migratory traits across species. In Paper IV, we generated a willow warbler karyotype to locate the MARB region, which explains most variation in migratory direction. We screened the genome of two other migratory Phylloscopus taxa, the common chiffchaff P. collybita and the greenish warbler P. trohiloides, for comparative analyses. Such analyses also revealed a high amount of intact olfactory receptor sequences, posing the question whether olfaction may play a role in migratory direction. In Paper V we combine geolocator data and genomic analyses in the closest relative to willow warbler, the common chiffchaff, and we built a model that best explains the demographic history of two of its subspecies. In Paper VI we studied migratory differences between two chiffchaff species, which are sister taxa, the Iberian chiffchaff P. ibericus and the common chiffchaff, which occur in northern Spain. We use pressure geolocators which provide us with high resolution tracks, allowing for a more detailed comparison of their very distinct migratory behaviour. Hence, my thesis constitutes a big leap in the understanding of the proximal mechanisms behind migratory behaviour in birds, especially in relation to complex genomic regions and migratory routes.