Elucidating the genomic basis of fitness variation in a long-lived polymorphic predator

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Fitness variation in wild species commonly depends on many complex traits and is therefore hard to understand in terms of ecological and molecular mechanisms. In contrast to this presumed general picture, fitness in some clades mainly correlates with one simple trait. Such a case is present in the common buzzard Buteo buteo and many other bird of prey of the order Accipitriformes. Here, the genetically encoded colour morph is the major determinant of lifetime reproductive success and has a Mendelian inheritance pattern, corresponding to one locus with two alleles. Our long-term datasets show that colour morph in buzzards correlates with many traits which may contribute to the differential fitness, including host-parasite interactions, immune defences, migration and aggressive behavior. This provides three alternative hypotheses how these correlations can arise: 1. A single nucleotide polymorphism (SNP) within a member gene of the melanisation pathway affects different traits. 2. Several SNPs within interaction partners having pleiotropic effects on melanisation and other traits and 3. A chromosomal inversion linking variation among functionally unrelated genes and their dependent traits. This project will use genomic tools to gather decisive evidence for one of these hypotheses and address the colour polymorphism and fitness variation in all birds of prey and the common buzzard as a focal species in a top-down approach. The first step of the project will use multiple platforms for sequencing long and linked reads, as well as optical mapping, to construct chromosome-level reference genomes of the different buzzard morphs. The hybrid assembly will produce, as a by-product, a highly valuable and rare genomic resource - the genome of the malaria-related blood parasite of buzzards, Leucocytozoon toddi. The high-quality reference genomes will be used as mapping targets for short-read sequences from many individuals of common buzzard and representatives of other polymorphic and monomorphic birds of prey. The resulting data will be deployed in genome-wide association studies and singleton-based selection analyses, revealing the genomic regions corresponding to morph and fitness variation in buzzards in detail, but also in their blood parasites and in other raptor taxa as a general pattern. Eventually, this project will reveal the genomic regions responsible for the colour polymorphism in common buzzards and will predict the traits which should correlate with colour because of pleiotropy or linkage. Furthermore, we will discover whether polymorphisms have arisen on multiple instances or whether this genomic variation is universal in the order of raptors and has played a key role for their fast speciation.