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 ...
How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (Myr) of divergence and degeneration obscure their evolutionary history. The Sylvioidea group of songbirds is interesting for understanding avian sex chromosome evolution because a chromosome fusion event ∼24 Myr ago formed “neo-sex chromosomes” consisting of an added (new) and an ancestral (old) part. Here, we report the complete female genome (ZW) of one Sylvioidea species, the great reed warbler (Acrocephalus arundinaceus). Our long-read assembly shows that the added region has been translocated to both Z and W, and while the added-Z has remained its gene order the added-W part has been heavily rearranged. Phylogenetic analyses show that recombination between the homologous added-Z and -W regions continued after the fusion event, and that recombination suppression across this region took several million years to be completed. Moreover, recombination suppression was initiated across multiple positions over the added-Z, which is not consistent with a simple linear progression starting from the fusion point. As expected following recombination suppression, the added-W show signs of degeneration including repeat accumulation and gene loss. Finally, we present evidence for non-random maintenance of slowly evolving and dosage-sensitive genes on both ancestral- and added-W, a process causing correlated evolution among orthologous genes across broad taxonomic groups, regardless of sex-linkage.
Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits (Parus major) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.
Heterogeneous patterns of genomic differentiation are commonly documented between closely related populations and there is considerable interest in identifying factors that contribute to their formation. These factors could include genomic features (e.g., areas of low recombination) that promote processes like linked selection (positive or purifying selection that affects linked neutral sites) at specific genomic regions. Examinations of repeatable patterns of differentiation across population pairs can provide insight into the role of these factors. Birds are well suited for this work, as genome structure is conserved across this group. Accordingly, we reestimated relative (FST) and absolute (dXY) differentiation between eight sister pairs of birds that span a broad taxonomic range using a common pipeline. Across pairs, there were modest but significant correlations in window‐based estimates of differentiation (up to 3% of variation explained for FST and 26% for dXY), supporting a role for processes at conserved genomic features in generating heterogeneous patterns of differentiation; processes specific to each episode of population divergence likely explain the remaining variation. The role genomic features play was reinforced by linear models identifying several genomic variables (e.g., gene densities) as significant predictors of FST and dXY repeatability. FST repeatability was higher among pairs that were further along the speciation continuum (i.e., more reproductively isolated) providing further insight into how genomic differentiation changes with population divergence; early stages of speciation may be dominated by positive selection that is different between pairs but becomes integrated with processes acting according to shared genomic features as speciation proceeds.
BackgroundAnimal migration requires adaptations in morphological, physiological and behavioural traits. Several of these traits have been shown to possess a strong heritable component in birds, but little is known about their genetic architecture. Here we used 454 sequencing of brain-derived transcriptomes from two differentially migrating subspecies of the willow warbler Phylloscopus trochilus to detect genes potentially underlying traits associated with migration.ResultsThe transcriptome sequencing resulted in 1.8 million reads following filtering steps. Most of the reads (84%) were successfully mapped to the genome of the zebra finch Taeniopygia gutatta. The mapped reads were situated within at least 12,101 predicted zebra finch genes, with the greatest sequencing depth in exons. Reads that were mapped to intergenic regions were generally located close to predicted genes and possibly located in uncharacterized untranslated regions (UTRs). Out of 85,000 single nucleotide polymorphisms (SNPs) with a minimum sequencing depth of eight reads from each of two subspecies-specific pools, only 55 showed high differentiation, confirming previous studies showing that most of the genetic variation is shared between the subspecies. Validation of a subset of the most highly differentiated SNPs using Sanger sequencing demonstrated that several of them also were differentiated between an independent set of individuals of each subspecies. These SNPs were clustered in two chromosome regions that are likely to be influenced by divergent selection between the subspecies and that could potentially be associated with adaptations to their different migratory strategies.ConclusionsOur study represents the first large-scale sequencing analysis aiming at detecting genes underlying migratory phenotypes in birds and provides new candidates for genes potentially involved in migration.
BackgroundWe still have limited knowledge about the underlying genetic mechanisms that enable migrating species of birds to navigate the globe. Here we make an attempt to get insight into the genetic architecture controlling this complex innate behaviour. We contrast the gene expression profiles of two closely related songbird subspecies with divergent migratory phenotypes. In addition to comparing differences in migratory strategy we include a temporal component and contrast patterns between breeding adults and autumn migrating juvenile birds of both subspecies. The two willow warbler subspecies, Phylloscopus trochilus trochilus and P. t. acredula, are remarkably similar both in phenotype and genotype and have a narrow contact zone in central Scandinavia. Here we used a microarray gene chip representing 23,136 expressed sequence tags (ESTs) from the zebra finch Taeniopygia guttata to identify mRNA level differences in willow warbler brain tissue in relation to subspecies and season.ResultsOut of the 22,109 EST probe sets that remained after filtering poorly binding probes, we found 11,898 (51.8 %) probe sets that could be reliably and uniquely matched to a total of 6,758 orthologous zebra finch genes. The two subspecies showed very similar levels of gene expression with less than 0.1 % of the probe sets being significantly differentially expressed. In contrast, 3,045 (13.8 %) probe sets were found to be differently regulated between samples collected from breeding adults and autumn migrating juvenile birds. The genes found to be differentially expressed between seasons appeared to be enriched for functional roles in neuronal firing and neuronal synapse formation.ConclusionsOur results show that only few genes are differentially expressed between the subspecies. This suggests that the different migration strategies of the subspecies might be governed by few genes, or that the expression patterns of those genes are time-structured or tissue-specific in ways, which our approach fails to uncover. Our findings will be useful in the planning of new experiments designed to unravel the genes involved in the migratory program of birds.Electronic supplementary materialThe online version of this article (doi:10.1186/s40462-016-0069-6) contains supplementary material, which is available to authorized users.
No abstract
2Heterogeneous patterns of genomic differentiation are commonly documented between 20 closely related populations and there is considerable interest in identifying factors that 21 contribute to their formation. These factors could include genomic features (e.g., areas of low 22 recombination) that promote processes like linked selection (positive or purifying selection 23 that affects linked neutral sites) at specific genomic regions. Examinations of repeatable 24 patterns of differentiation across population pairs can provide insight into the role of these 25 factors. Birds are well suited for this work, as genome structure is conserved across this 26 group. Accordingly, we re-estimated relative (F ST ) and absolute (d XY ) differentiation between 27 eight sister pairs of birds that span a broad taxonomic range using a common pipeline. Across 28 pairs, there were modest but significant correlations in window-based estimates of 29 differentiation (up to 3% of variation explained for F ST and 26% for d XY ), supporting a role for 30 processes at conserved genomic features in generating heterogeneous patterns of 31 differentiation. This suggestion was reinforced by linear models identifying several genomic 32 features (e.g., gene densities) as significant predictors of F ST and d XY repeatability. F ST 33 repeatability was higher among pairs that were further along the speciation continuum (i.e., 34 more reproductively isolated), suggesting that early stages of speciation may be dominated by 35 positive selection that is different between pairs and replaced by processes acting according to 36 shared genomic features as speciation proceeds. 37 peer-reviewed)
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