Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks

Abstract

It is well established that differences in migratory behavior between populations of songbirds have a genetic basis but the actual genes underlying these traits remains largely unknown. In an attempt to identify such candidate genes we de novo assembled the genome of the willow warbler Phylloscopus trochilus, and used whole-genome resequencing and a SNP array to associate genomic variation with migratory phenotypes across two migratory divides around the Baltic Sea that separate SW migrating P. t. trochilus wintering in western Africa and SSE migrating P. t. acredula wintering in eastern and southern Africa. We found that the genomes of the two migratory phenotypes lack clear differences except for three highly differentiated regions located on chromosomes 1, 3, and 5 (containing 146, 135, and 53 genes, respectively). Within each migratory phenotype we found virtually no differences in allele frequencies for thousands of SNPs, even when comparing geographically distant populations breeding in Scandinavia and Far East Russia (>6000 km). In each of the three differentiated regions, multidimensional scaling-based clustering of SNP genotypes from more than 1100 individuals demonstrates the presence of distinct haplotype clusters that are associated with each migratory phenotype. In turn, this suggests that recombination is absent or rare between haplotypes, which could be explained by inversion polymorphisms. Whereas SNP alleles on chromosome 3 correlate with breeding altitude and latitude, the allele distribution within the regions on chromosomes 1 and 5 perfectly matches the geographical distribution of the migratory phenotypes. The most differentiated 10 kb windows and missense mutations within these differentiated regions are associated with genes involved in fatty acid synthesis, possibly representing physiological adaptations to the different migratory strategies.The ß200 genes in these regions, of which several lack described function, will direct future experimental and comparative studies in the search for genes that underlie important migratory traits. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Evolution Letters 1-3: 155-168MAX LUNDBERG ET AL. Impact SummaryHow animals find their way when migrating between continents is one of the most fascinating phenomena in nature. It is well established that migratory behavior has a strong genetic basis in many bird species, and different routes and wintering areas are also likely to select for adaptations related to optimal migratory performance, such as changes in physiology. However, virtually nothing is known about the specific genes underlying these traits. Here we aim to detect migration genes by contrasting the genomes of two recently diverged populations of a small migratory songbird, the willow warbler, which are very similar in appearance but that differ markedly in migration routes and wintering areas ...

The genetics and epigenetics of animal migration and orientation: birds, butterflies and beyond

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