An integrative study of bird migration : From the migratory phenotype to its gene regulation mechanisms and back.

Life goes out of equilibrium; it is in constant movement. Animals, especially, move as part of their life cycle. An outstanding example is bird migration. Some birds adopt migration as a strategy to survive the harsh conditions of weather seasonality in temperate regions. Different sources of evidence indicate that seasonal migration is innate, and it can be inherited. Mutations in such heritable behaviour create an array of diversity in migratory traits: timing, orientation and distance. The diversity of migratory traits can affect ecological speciation. Migratory divides, for instance, are geographical areas where birds with different migratory orientations hybridise. If the differences in migratory behaviour are strong enough to create reproductive barriers, this could evolve into population divergence and eventually, speciation. However, to understand the potential processes of divergence caused by migratory behaviours, a crucial element is missing: the identity of the molecular mechanisms involved in migration. Genome-wide studies in bird species with migratory divides find several different genomic regions with species-specific signature. Similarly, gene expression approaches in different organs and species find groups of individual differentially expressed genes. These results suggest an intricate mechanism for the genetics of migration with potential species-specific characteristics. This thesis analyses the migratory behaviour from different angles spanning the phenotype to gene regulation, to contribute to the identification of mechanisms and evolution of migration. Most of the chapters of this thesis use the Eurasian blackcap ( Sylvia atricapilla) a species that comprise an extensive repertoire of orientation and distance traits, including entirely resident populations. With blackcaps, we studied the phenotypic variability of migration tracking individuals ithroughout the year (Chapter 2). We used light-level geolocators to obtain migratory routes of individuals from populations in Central Europe and the United Kingdom. We describe for the first time the orientation and timing patterns of individuals from a migratory divide and a recently adapted population in the UK. In chapter 4, we analyse the genomics and evolution patterns of blackcaps. Using whole-genome resequencing of populations covering all the differences in migratory traits, we describe population structure and demography in this species. We found that blackcaps show very little genomic differentiation. The most divergent populations are residents, while migratory populations comprise a single population at the genetic level. Chapter 5 is the first study of gene regulatory mechanisms in the context of bird migration. We characterised the chromatin accessibility landscape in three brain areas contrasting individuals during migration with individuals out of the migratory season. One of the findings is a general pattern of gene repression in relevant brain regions like the Cluster N. Moreover; we found cis-regulatory modules with particular evolutionary trajectories that may play a role in migration. Lastly, we did two comparative approaches to study macroevolutionary patterns related to migration. First, we analysed phylogenetic patterns and structural characteristics of previously proposed candidate genes (chapter 3). We found that the candidate genes do not have structural characteristics correlated with the presence of migration across the avian clade as it does within some species. The second comparative approach (Chapter 6), evaluates the repeatability patterns of genomic divergence in pairs of populations from migratory divides. Our results suggests that the degree of repeatability is mainly driven by how apart in the speciation continuum is the population pair located: if the pair is recently diverging, iifew repeatability is detected, while if the populations are further apart, repeatability is more plausible. Overall, this thesis highlights an essential feature for the study of complex traits like migration: integration of different sources of evidence. Ideally, in these cases, the analysis of phenotype, evolutionary patterns and regulatory mechanisms in the same individuals, should be the standard procedure. We are aware that this is an implausible scenario. However, the integration of different studies, help to guide the search of molecular elements involved in bird migration. This thesis is the first - at least that we are aware of - study compilating research on a variety of topics to understand bird migration. We are still far from getting a definitive understanding of bird migration. Nevertheless, confirming the heritability of the phenotype, describing macro and microevolutionary patterns of migration and specific regulatory elements, will improve the search for new candidate genes for this behaviour


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