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Avian long-distance migration requires refined programming to orchestrate the birds' movements on annual temporal and continental spatial scales. Programming is particularly important as long-distance movements typically anticipate future environmental conditions. Hence, migration has long been of particular interest in chronobiology. Captivity studies using a proxy, the shift to nocturnality during migration seasons (i.e., migratory restlessness), have revealed circannual and circadian regulation, as well as an innate sense of direction. Thanks to rapid development of tracking technology, detailed information from free-flying birds, including annual-cycle data and actograms, now allows relating this mechanistic background to behaviour in the wild. Likewise, genomic approaches begin to unravel the many physiological pathways that contribute to migration. Despite these advances, it is still unclear how migration programmes are integrated with specific environmental conditions experienced during the journey. Such knowledge is imminently important as temporal environments undergo rapid anthropogenic modification. Migratory birds as a group are not dealing well with the changes, yet some species show remarkable adjustments at behavioural and genetic levels. Integrated research programmes and interdisciplinary collaborations are needed to understand the range of responses of migratory birds to environmental change, and more broadly, the functioning of timing programmes under natural conditions.
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Migração Animal , Aves , Ritmo Circadiano , Animais , Migração Animal/fisiologia , Aves/fisiologia , Ritmo Circadiano/fisiologia , Estações do Ano , Relógios Biológicos/fisiologiaRESUMO
Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, and Cry4a from a migratory songbird seems to show enhanced magnetic sensitivity in vitro compared to Cry4a from resident species. We investigate Cry and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modelling. Our analysis is based on 363 bird genomes and identifies different selection regimes in passerines. We show that Cry4a is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that are likely to have facilitated the evolution of an optimized sensory protein for night-time orientation in songbirds. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines), and thus identified a gene deletion, which might facilitate testing the function of Cry4a in birds. In contrast, the other avian Cry (Cry1 and Cry2) were highly conserved across all species, indicating basal, non-sensory functions. Our results support a specialization or functional differentiation of Cry4 in songbirds which could be magnetosensation.
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Aves Canoras , Animais , Filogenia , Aves Canoras/fisiologia , Criptocromos/metabolismo , Campos Magnéticos , Migração Animal/fisiologiaRESUMO
Recombination is responsible for breaking up haplotypes, influencing genetic variability, and the efficacy of selection. Bird genomes lack the protein PR domain-containing protein 9, a key determinant of recombination dynamics in most metazoans. Historical recombination maps in birds show an apparent stasis in positioning recombination events. This highly conserved recombination pattern over long timescales may constrain the evolution of recombination in birds. At the same time, extensive variation in recombination rate is observed across the genome and between different species of birds. Here, we characterize the fine-scale historical recombination map of an iconic migratory songbird, the Eurasian blackcap (Sylvia atricapilla), using a linkage disequilibrium-based approach that accounts for population demography. Our results reveal variable recombination rates among and within chromosomes, which associate positively with nucleotide diversity and GC content and negatively with chromosome size. Recombination rates increased significantly at regulatory regions but not necessarily at gene bodies. CpG islands are associated strongly with recombination rates, though their specific position and local DNA methylation patterns likely influence this relationship. The association with retrotransposons varied according to specific family and location. Our results also provide evidence of heterogeneous intrachromosomal conservation of recombination maps between the blackcap and its closest sister taxon, the garden warbler. These findings highlight the considerable variability of recombination rates at different scales and the role of specific genomic features in shaping this variation. This study opens the possibility of further investigating the impact of recombination on specific population-genomic features.
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Genômica , Aves Canoras , Animais , Aves Canoras/genética , Ilhas de CpG , Metilação de DNA , Recombinação GenéticaRESUMO
Structural variants (SVs) are a major source of genetic variation; and descriptions in natural populations and connections with phenotypic traits are beginning to accumulate in the literature. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (a) characterized the genome-wide distribution, frequency, and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (b) used these SVs to study the genetics of seasonal migration. We detected >15 K SVs. Many SVs overlapped repetitive regions and exhibited evidence of purifying selection suggesting they have overall deleterious effects on fitness. We used estimates of genomic differentiation to identify SVs exhibiting evidence of selection in blackcaps with different migratory strategies. Insertions and deletions dominated the SVs we identified and were associated with genes that are either directly (e.g., regulatory motifs that maintain circadian rhythms) or indirectly (e.g., through immune response) related to migration. We also broke migration down into individual traits (direction, distance, and timing) using existing tracking data and tested if genetic variation at the SVs we identified could account for phenotypic variation at these traits. This was only the case for 1 trait-direction-and 1 specific SV (a deletion on chromosome 27) accounted for much of this variation. Our results highlight the evolutionary importance of SVs in natural populations and provide insight into the genetic basis of seasonal migration.
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Birds in seasonal habitats rely on intricate strategies for optimal timing of migrations. This is governed by environmental cues, including photoperiod. Genetic factors affecting intrinsic timekeeping mechanisms, such as circadian clock genes, have been explored, yielding inconsistent findings with potential lineage-dependency. To clarify this evidence, a systematic review and phylogenetic reanalysis was done. This descriptor outlines the methodology for sourcing, screening, and processing relevant literature and data. PRISMA guidelines were followed, ultimately including 66 studies, with 34 focusing on candidate genes at the genotype-phenotype interface. Studies were clustered using bibliographic coupling and citation network analysis, alongside scientometric analyses by publication year and location. Data was retrieved for allele data from databases, article supplements, and direct author communications. The dataset, version 1.0.2, encompasses data from 52 species, with 46 species for the Clock gene and 43 for the Adcyap1 gene. This dataset, featuring data from over 8000 birds, constitutes the most extensive cross-species collection for these candidate genes, used in studies investigating gene polymorphisms and seasonal bird migration.
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Migração Animal , Proteínas Aviárias , Aves , Alelos , Ritmo Circadiano/genética , Fotoperíodo , Filogenia , Polimorfismo Genético , Revisões Sistemáticas como Assunto , Animais , Proteínas Aviárias/genética , Migração Animal/fisiologiaRESUMO
Transposable elements (TEs) are mobile genetic elements that can move around the genome, and as such are a source of genomic variability. Based on their characteristics we can annotate TEs within the host genome and classify them into specific TE types and families. The increasing number of available high-quality genome references in recent years provides an excellent resource that will enhance the understanding of the role of recently active TEs on genetic variation and phenotypic evolution. Here we showcase the use of a high-quality TE annotation to understand the distinct effect of recent and ancient TE insertions on the evolution of genomic variation, within our study species the Eurasian blackcap (Sylvia atricapilla). We investigate how these distinct TE categories are distributed along the genome and evaluate how their coverage across the genome is correlated with four genomic features: recombination rate, gene coverage, CpG island coverage and GC content. We found within the recent TE insertions an accumulation of LTRs previously not seen in birds. While the coverage of recent TE insertions was negatively correlated with both GC content and recombination rate, the correlation with recombination rate disappeared and turned positive for GC content when considering ancient TE insertions.
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Genoma , Retroelementos , Humanos , Retroelementos/genética , Genômica , Sequências Repetidas Terminais/genética , Ilhas de CpG , Elementos de DNA Transponíveis/genética , Evolução MolecularRESUMO
The ability of migratory birds to sense magnetic fields has been known for decades, although the understanding of the underlying mechanism is still elusive. Currently, the strongest magnetoreceptor candidate in birds is a protein called cryptochrome 4a. The cryptochrome 4a protein has changed through evolution, apparently endowing some birds with a more pronounced magnetic sensitivity than others. Using phylogenetic tools, we show that a specific tryptophan tetrad and a tyrosine residue predicted to be essential for cryptochrome activation are highly conserved in the avian clade. Through state-of-the-art molecular dynamics simulations and associated analyses, we also studied the role of these specific residues and the associated mutants on the overall dynamics of the protein. The analyses of the single residue mutations were used to judge how far a local change in the protein structure can impact specific dynamics of European robin cryptochrome 4a. We conclude that the replacements of each of the tryptophans one by one with a phenylalanine do not compromise the overall stability of the protein.
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Given that all interactions between an animal and its environment are mediated by movement, questions of how animals inherit, refine and execute trajectories through space are fundamental to our understanding of biology. As with any behavioural trait, navigation can be thought of on many conceptual levels - from the mechanistic to the functional, and from the static to the dynamic - as laid out by Niko Tinbergen in his four questions of animal behaviour. Here, we use a navigation-centric interpretation of Tinbergen's questions to summarise and critique advances in the field of animal navigation. We discuss the 'state of the art'; consider how a proximal/mechanistic understanding of navigation is not a prerequisite to understanding ultimate questions of evolutionary/adaptive importance; propose that certain aspects of animal navigation research - and certain taxa - are being neglected; and suggest that extreme experimental manipulations might lead to the mischaracterisation of non-adaptive 'spandrels' as functional navigational mechanisms. More generally, we highlight pressing questions within the field, the answers to which we believe are within reach, and highlight the important role that novel methods will have in helping us elucidate them.
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Comportamento Animal , Navegação Espacial , Animais , Evolução Biológica , Fenótipo , MovimentoRESUMO
Timing is a crucial aspect for survival and reproduction in seasonal environments leading to carefully scheduled annual programs of migration in many species. But what are the exact mechanisms through which birds (class: Aves) can keep track of time, anticipate seasonal changes, and adapt their behaviour? One proposed mechanism regulating annual behaviour is the circadian clock, controlled by a highly conserved set of genes, collectively called 'clock genes' which are well established in controlling the daily rhythmicity of physiology and behaviour. Due to diverse migration patterns observed within and among species, in a seemingly endogenously programmed manner, the field of migration genetics has sought and tested several candidate genes within the clock circuitry that may underlie the observed differences in breeding and migration behaviour. Among others, length polymorphisms within genes such as Clock and Adcyap1 have been hypothesised to play a putative role, although association and fitness studies in various species have yielded mixed results. To contextualise the existing body of data, here we conducted a systematic review of all published studies relating polymorphisms in clock genes to seasonality in a phylogenetically and taxonomically informed manner. This was complemented by a standardised comparative re-analysis of candidate gene polymorphisms of 76 bird species, of which 58 are migrants and 18 are residents, along with population genetics analyses for 40 species with available allele data. We tested genetic diversity estimates, used Mantel tests for spatial genetic analyses, and evaluated relationships between candidate gene allele length and population averages for geographic range (breeding- and non-breeding latitude), migration distance, timing of migration, taxonomic relationships, and divergence times. Our combined analysis provided evidence (i) of a putative association between Clock gene variation and autumn migration as well as a putative association between Adcyap1 gene variation and spring migration in migratory species; (ii) that these candidate genes are not diagnostic markers to distinguish migratory from sedentary birds; and (iii) of correlated variability in both genes with divergence time, potentially reflecting ancestrally inherited genotypes rather than contemporary changes driven by selection. These findings highlight a tentative association between these candidate genes and migration attributes as well as genetic constraints on evolutionary adaptation.
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Migração Animal , Aves , Animais , Migração Animal/fisiologia , Aves/genética , Polimorfismo Genético , Genótipo , Evolução Biológica , Estações do AnoRESUMO
Methylation of cytosines is a prototypic epigenetic modification of the DNA. It has been implicated in various regulatory mechanisms across the animal kingdom and particularly in vertebrates. We mapped DNA methylation in 580 animal species (535 vertebrates, 45 invertebrates), resulting in 2443 genome-scale DNA methylation profiles of multiple organs. Bioinformatic analysis of this large dataset quantified the association of DNA methylation with the underlying genomic DNA sequence throughout vertebrate evolution. We observed a broadly conserved link with two major transitions-once in the first vertebrates and again with the emergence of reptiles. Cross-species comparisons focusing on individual organs supported a deeply conserved association of DNA methylation with tissue type, and cross-mapping analysis of DNA methylation at gene promoters revealed evolutionary changes for orthologous genes. In summary, this study establishes a large resource of vertebrate and invertebrate DNA methylomes, it showcases the power of reference-free epigenome analysis in species for which no reference genomes are available, and it contributes an epigenetic perspective to the study of vertebrate evolution.
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Metilação de DNA , Genoma , Animais , Metilação de DNA/genética , Genoma/genética , Invertebrados/genética , Vertebrados/genética , Vertebrados/metabolismo , Epigênese Genética , DNA/metabolismoRESUMO
A recent study by Xu et al. (Nature, 2021, 594, 535-540) provided strong evidence that cryptochrome 4 (Cry4) is a key protein to endow migratory birds with the magnetic compass sense. The investigation compared the magnetic field response of Cry4 from migratory and nonmigratory bird species and suggested that a difference in magnetic sensitivity could exist. This finding prompted an in-depth investigation into Cry4 protein differences on the structural and dynamic levels. In the present study, the pigeon Cry4 (ClCry4) crystal structure was used to reconstruct the missing avian Cry4 protein structures via homology modeling for carefully selected bird species. The reconstructed Cry4 structure from European robin, Eurasian blackcap, zebra finch, chicken, and pigeon were subsequently simulated dynamically and analyzed. The studied avian Cry4 structures show flexibility in analogous regions pointing to similar activation mechanisms and/or signaling interaction partners. It can be concluded that the experimentally recorded difference in the magnetic field sensitivity of Cry4 from different birds is unlikely to be due to solely intrinsic dynamics of the proteins but requires additional factors that have not yet been identified.
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Proteínas Aviárias , Aves Canoras , Animais , Proteínas Aviárias/metabolismo , Criptocromos/química , Campos Magnéticos , Modelos Estruturais , Aves Canoras/metabolismoRESUMO
Timing is essential for survival and reproduction of organisms across the tree of life. The core circadian clock gene Clk is involved in the regulation of annual timing events and shows highly conserved sequence homology across vertebrates except for one variable region of poly-glutamine repeats. Clk genotype varies in some species with latitude, seasonal timing and migration. However, findings are inconsistent, difficult to disentangle from environmental responses, and biased towards high latitudes. Here we combine field data with a common-garden experiment to study associations of Clk polymorphism with latitude, migration and annual-cycle timing within the stonechat species complex across its trans-equatorial distribution range. Our dataset includes 950 records from 717 individuals from nine populations with diverse migratory strategies. Gene diversity was lowest in resident African and Canary Island populations and increased with latitude, independently of migration distance. Repeat length and annual-cycle timing was linked in a population-specific way. Specifically, equatorial African stonechats showed delayed timing with longer repeat length for all annual-cycle stages. Our data suggest that at low latitudes with nearly constant photoperiod, Clk genotype might orchestrate a range of consistent, individual chronotypes. In contrast, the influence of Clk on annual-cycle timing at higher latitudes might be mediated by its interactions with genes involved in (circadian) photoperiodic pathways.
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Relógios Circadianos , Fotoperíodo , Animais , Ritmo Circadiano , Polimorfismo Genético , ReproduçãoRESUMO
How local phenotypic variation is maintained in highly mobile organisms, like birds, is an open question. A new study shows that a massive chromosomal inversion underlies a polymorphism in common quail.
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Inversão Cromossômica , Codorniz , Animais , Evolução Biológica , Polimorfismo Genético , Codorniz/genética , Recombinação GenéticaRESUMO
Understanding the points in a species breeding cycle when they are most vulnerable to environmental fluctuations is key to understanding interannual demography and guiding effective conservation and management. Seabirds represent one of the most threatened groups of birds in the world, and climate change and severe weather is a prominent and increasing threat to this group. We used a multi-state capture-recapture model to examine how the demographic rates of a long-lived trans-oceanic migrant seabird, the Manx shearwater Puffinus puffinus, are influenced by environmental conditions experienced at different stages of the annual breeding cycle and whether these relationships vary with an individual's breeding state in the previous year (i.e., successful breeder, failed breeder and non-breeder). Our results imply that populations of Manx shearwaters are comprised of individuals with different demographic profiles, whereby more successful reproduction is associated with higher rates of survival and breeding propensity. However, we found that all birds experienced the same negative relationship between rates of survival and wind force during the breeding season, indicating a cost of reproduction (or central place constraint for non-breeders) during years with severe weather conditions. We also found that environmental effects differentially influence the breeding propensity of individuals in different breeding states. This suggests individual spatio-temporal variation in habitat use during the annual cycle, such that climate change could alter the frequency that individuals with different demographic profiles breed thereby driving a complex and less predictable population response. More broadly, our study highlights the importance of considering individual-level factors when examining population demography and predicting how species may respond to climate change.
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Migração Animal/fisiologia , Cruzamento , Mudança Climática , Demografia/estatística & dados numéricos , Ecossistema , Reprodução , Estações do Ano , Animais , Aves , Oceanos e MaresRESUMO
Human behavior profoundly affects the natural world. Migratory birds are particularly susceptible to adverse effects of human activities because the global networks of ecosystems on which birds rely are undergoing rapid change. In spite of these challenges, the blackcap (Sylvia atricapilla) is a thriving migratory species. Its recent establishment of high-latitude wintering areas in Britain and Ireland has been linked to climate change and backyard bird feeding, exemplifying the interaction between human activity and migrant ecology. To understand how anthropogenic influences shape avian movements and ecology, we marked 623 wintering blackcaps at 59 sites across Britain and Ireland and compiled a dataset of 9929 encounters. We investigated visitation behavior at garden feeding sites, inter-annual site fidelity, and movements within and across seasons. We analyzed migration tracks from 25 geolocators fitted to a subset of individuals to understand how garden behavior may impact subsequent migration and breeding. We found that blackcaps wintering in Britain and Ireland showed high site fidelity and low transience among wintering sites, in contrast to the itinerant movements characteristic of blackcaps wintering in their traditional winter range. First-winter birds showed lower site fidelity and a greater likelihood of transience than adults. Adults that frequented gardens had better body condition, smaller fat stores, longer bills, and rounder wingtips. However, blackcaps did not exclusively feed in gardens; visits were linked to harsher weather. Individuals generally stayed at garden sites until immediately before spring departure. Our results suggest that supplementary feeding is modifying blackcap winter ecology and driving morphological evolution. Supplemental feeding may have multifaceted benefits on winter survival, and these positive effects may carry over to migration and subsequent breeding. Overall, the high individual variability in blackcap movement and foraging ecology, and the flexibility it imparts, may have allowed this species to flourish during rapid environmental change.
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Migração Animal , Ecossistema , Animais , Atividades Humanas , Humanos , Irlanda , Estações do AnoRESUMO
Supergenes are regions of suppressed recombination that may span hundreds of genes and can control variation in key ecological phenotypes. Since genetic analysis is made impossible by the absence of recombination between genes, it has been difficult to establish how individual genes within these regions contribute to supergene-controlled phenotypes. The white-throated sparrow is a classic example in which a supergene controls behavioral differences as well as distinct coloration that determines mate choice. A landmark study now demonstrates that differences between supergene variants in the promoter sequences of a hormone receptor gene change its expression and control changes in behavior. To unambiguously establish the link between genotype and phenotype, the authors used antisense oligonucleotides to alter the level of gene expression in a focal brain region targeted through a cannula. The study showcases a powerful approach to the functional genomic manipulation of a wild vertebrate species.
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Seasonal migration is a complex and variable behaviour with the potential to promote reproductive isolation. In Eurasian blackcaps (Sylvia atricapilla), a migratory divide in central Europe separating populations with southwest (SW) and southeast (SE) autumn routes may facilitate isolation, and individuals using new wintering areas in Britain show divergence from Mediterranean winterers. We tracked 100 blackcaps in the wild to characterize these strategies. Blackcaps to the west and east of the divide used predominantly SW and SE directions, respectively, but close to the contact zone many individuals took intermediate (S) routes. At 14.0° E, we documented a sharp transition from SW to SE migratory directions across only 27 (10-86) km, implying a strong selection gradient across the divide. Blackcaps wintering in Britain took northwesterly migration routes from continental European breeding grounds. They originated from a surprisingly extensive area, spanning 2000 km of the breeding range. British winterers bred in sympatry with SW-bound migrants but arrived 9.8 days earlier on the breeding grounds, suggesting some potential for assortative mating by timing. Overall, our data reveal complex variation in songbird migration and suggest that selection can maintain variation in migration direction across short distances while enabling the spread of a novel strategy across a wide range.
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Migração Animal , Passeriformes , Animais , Evolução Biológica , Europa (Continente) , Isolamento Reprodutivo , Aves CanorasRESUMO
Seasonal migration is a taxonomically widespread behaviour that integrates across many traits. The European blackcap exhibits enormous variation in migration and is renowned for research on its evolution and genetic basis. We assembled a reference genome for blackcaps and obtained whole genome resequencing data from individuals across its breeding range. Analyses of population structure and demography suggested divergence began ~30,000 ya, with evidence for one admixture event between migrant and resident continent birds ~5000 ya. The propensity to migrate, orientation and distance of migration all map to a small number of genomic regions that do not overlap with results from other species, suggesting that there are multiple ways to generate variation in migration. Strongly associated single nucleotide polymorphisms (SNPs) were located in regulatory regions of candidate genes that may serve as major regulators of the migratory syndrome. Evidence for selection on shared variation was documented, providing a mechanism by which rapid changes may evolve.
Every year as the seasons change, thousands of animals migrate huge distances in search of food or better climates. As far as migrations go, there might be none so impressive as the trans-oceanic flights made by small migrating songbirds. These birds can weigh as little as three grams and travel up to 15,000 kilometres. Most migrate alone and at night and yet still manage to return to the same location each year. Several strands of research suggest there could be a genetic basis to their migratory behaviour, but exactly which genes control this phenomenon remains poorly understood. One small songbird that has been studied for decades is the European blackcap. This species exhibits a real variety of migration patterns. Some blackcaps travel rather short distances, others much further, and some populations do not migrate at all. Populations that share the same breeding grounds in the summer may migrate in different directions in the autumn. These features make it a good species to study the genetic variation between populations that migrate in different directions and over different distances. However, only in recent years has advancing technology made it possible to comprehensively study an animal's entire genome, leaving no gene unturned. Now, Delmore et al. have used high-throughput sequencing technologies to trace the evolutionary history of migration in European blackcap and started by assembling a reference genome for the species. Then, the genomes of 110 blackcaps from several populations that take different annual migrations were compared to the reference. This revealed that the populations began to diverge some 30,000 years ago and that there was some apparent gene mixing between groups of migrating and resident blackcaps around 5,000 years ago. The analysis showed only a small set of genes code for their differences in migration. Additionally, while the candidate genes were shown to be common among blackcaps, the genes identified did not match those reported from studies of other migrating songbirds. Finally, Delmore et al. also noted that the differences between the populations tend to be in the parts of the genome that control whether a given gene is switched on or off, which could explain how new migratory behaviours can rapidly evolve. This study is one of the most comprehensive genomic analysis of migration to date. It is important work as songbirds, like other animals, are responding to increasing pressures of environmental and climate change. In time, the findings could be used to support conservation efforts whereby genetic analyses could determine if certain populations possess enough variation to respond to coming changes in their habitats.