Genomics-informed conservation units reveal spatial variation in climate vulnerability in a migratory bird.

Identifying genetic conservation units (CUs) in threatened species is critical for the preservation of adaptive capacity and evolutionary potential in the face of climate change. However, delineating CUs in highly mobile species remains a challenge due to high rates of gene flow and genetic signatures of isolation by distance. Even when CUs are delineated in highly mobile species, the CUs often lack key biological information about what populations have the most conservation need to guide management decisions. Here we implement a framework for CU identification in the Canada Warbler (Cardellina canadensis), a migratory bird species of conservation concern, and then integrate demographic modelling and genomic offset to guide conservation decisions. We find that patterns of whole genome genetic variation in this highly mobile species are primarily driven by putative adaptive variation. Identification of CUs across the breeding range revealed that Canada Warblers fall into two evolutionarily significant units (ESU), and three putative adaptive units (AUs) in the South, East, and Northwest. Quantification of genomic offset, a metric of genetic changes necessary to maintain current gene-environment relationships, revealed significant spatial variation in climate vulnerability, with the Northwestern AU being identified as the most vulnerable to future climate change. Alternatively, quantification of past population trends within each AU revealed the steepest population declines have occurred within the Eastern AU. Overall, we illustrate that genomics-informed CUs provide a strong foundation for identifying current and future regional threats that can be used to inform management strategies for a highly mobile species in a rapidly changing world.

Genetic evidence for widespread population size expansion in North American boreal birds prior to the Last Glacial Maximum.

Pleistocene climate cycles are well documented to have shaped contemporary species distributions and genetic diversity. Northward range expansions in response to deglaciation following the Last Glacial Maximum (LGM; approximately 21 000 years ago) are surmised to have led to population size expansions in terrestrial taxa and changes in seasonal migratory behaviour. Recent findings, however, suggest that some northern temperate populations may have been more stable than expected through the LGM. We modelled the demographic history of 19 co-distributed boreal-breeding North American bird species from full mitochondrial gene sets and species-specific molecular rates. We used these demographic reconstructions to test how species with different migratory strategies were affected by glacial cycles. Our results suggest that effective population sizes increased in response to Pleistocene deglaciation earlier than the LGM, whereas genetic diversity was maintained throughout the LGM despite shifts in geographical range. We conclude that glacial cycles prior to the LGM have most strongly shaped contemporary genetic diversity in these species. We did not find a relationship between historic population dynamics and migratory strategy, contributing to growing evidence that major switches in migratory strategy during the LGM are unnecessary to explain contemporary migratory patterns.

Genomic approaches to mitigating genetic diversity loss in declining populations.

The accelerating pace of global biodiversity loss is exacerbated by habitat fragmentation and subsequent inbreeding in small populations. To address this problem, conservation practitioners often turn to assisted breeding programmes with the aim of enhancing genetic diversity in declining populations. Although genomic information is infrequently included in these efforts, it has the potential to significantly enhance the success of such programmes. In this study, we showcase the value of genomic approaches for increasing genetic diversity in assisted breeding efforts, specifically focusing on a highly inbred population of Western burrowing owls. To maximize genetic diversity in the resulting offspring, we begin by creating an optimal pairing decision tree based on sex, kinship and patterns of homozygosity across the genome. To evaluate the effectiveness of our strategy, we compare genetic diversity, brood size and nestling success rates between optimized and non-optimized pairs. Additionally, we leverage recently discovered correlations between telomere length and fitness across species to investigate whether genomic optimization could have long-term fitness benefits. Our results indicate that pairing individuals with contrasting patterns of homozygosity across the genome is an effective way to increase genetic diversity in offspring. Although short-term field-based metrics of success did not differ significantly between optimized and non-optimized pairs, offspring from optimized pairs had significantly longer telomeres, suggesting that genetic optimization can help reduce the risk of inbreeding depression. These findings underscore the importance of genomic tools for informing efforts to preserve the adaptive potential of small, inbred populations at risk of further decline.

Widespread gene flow following range expansion in Anna's Hummingbird.

Anthropogenic changes have altered the historical distributions of many North American taxa. As environments shift, ecological and evolutionary processes can combine in complex ways to either stimulate or inhibit range expansion. Here, we examined the role of evolution in a rapid range expansion whose ecological context has been well-documented, Anna's Hummingbird (Calypte anna). Previous studies have suggested that the C. anna range expansion is the result of an ecological release facilitated by human-mediated environmental changes, where access to new food sources have allowed further filling of the abiotic niche. We examined the role of gene flow and adaptation during range expansion from their native California breeding range, north into Canada and east into New Mexico and Texas, USA. Using low coverage whole genome sequencing we found high genetic diversity, low divergence, and little evidence of selection on the northern and eastern expansion fronts. Additionally, there are no clear barriers to gene flow across the native and expanded range. The lack of selective signals between core and expanded ranges could reflect (i) an absence of novel selection pressure in the expanded range (supporting the ecological release hypothesis), (ii) swamping of adaptive variation due to high gene flow, or (iii) limitations of genome scans for detecting small shifts in allele frequencies across many loci. Nevertheless, our results provide an example where strong selection is not apparent during a rapid, contemporary range shift.

Low-coverage whole genome sequencing for highly accurate population assignment: Mapping migratory connectivity in the American Redstart (Setophaga ruticilla).

Understanding the geographic linkages among populations across the annual cycle is an essential component for understanding the ecology and evolution of migratory species and for facilitating their effective conservation. While genetic markers have been widely applied to describe migratory connections, the rapid development of new sequencing methods, such as low-coverage whole genome sequencing (lcWGS), provides new opportunities for improved estimates of migratory connectivity. Here, we use lcWGS to identify fine-scale population structure in a widespread songbird, the American Redstart (Setophaga ruticilla), and accurately assign individuals to genetically distinct breeding populations. Assignment of individuals from the nonbreeding range reveals population-specific patterns of varying migratory connectivity. By combining migratory connectivity results with demographic analysis of population abundance and trends, we consider full annual cycle conservation strategies for preserving numbers of individuals and genetic diversity. Notably, we highlight the importance of the Northern Temperate-Greater Antilles migratory population as containing the largest proportion of individuals in the species. Finally, we highlight valuable considerations for other population assignment studies aimed at using lcWGS. Our results have broad implications for improving our understanding of the ecology and evolution of migratory species through conservation genomics approaches.

Evolutionary potential mitigates extinction risk under climate change in the endangered southwestern willow flycatcher.

The complexity of global anthropogenic change makes forecasting species responses and planning effective conservation actions challenging. Additionally, important components of a species' adaptive capacity, such as evolutionary potential, are often not included in quantitative risk assessments due to lack of data. While genomic proxies for evolutionary potential in at-risk species are increasingly available, they have not yet been included in extinction risk assessments at a species-wide scale. In this study, we used an individual-based, spatially explicit, dynamic eco-evolutionary simulation model to evaluate the extinction risk of an endangered desert songbird, the southwestern willow flycatcher (Empidonax traillii extimus), in response to climate change. Using data from long-term demographic and habitat studies in conjunction with genome-wide ecological genomics research, we parameterized simulations that include 418 sites across the breeding range, genomic data from 225 individuals, and climate change forecasts spanning 3 generalized circulation models and 3 emissions scenarios. We evaluated how evolutionary potential, and the lack of it, impacted population trajectories in response to climate change. We then investigated the compounding impact of drought and warming temperatures on extinction risk through the mechanism of increased nest failure. Finally, we evaluated how rapid action to reverse greenhouse gas emissions would influence population responses and species extinction risk. Our results illustrate the value of incorporating evolutionary, demographic, and dispersal processes in a spatially explicit framework to more comprehensively evaluate the extinction risk of threatened and endangered species and conservation actions to promote their recovery.

Where to draw the line? Expanding the delineation of conservation units to highly mobile taxa.

Conservation units (CUs) are an essential tool for maximizing evolutionary potential and prioritizing areas across a species' range for protection when implementing conservation and management measures. However, current workflows for identifying CUs on the basis of neutral and adaptive genomic variation largely ignore information contained in patterns of isolation by distance (IBD), frequently the primary signal of population structure in highly mobile taxa, such as birds, bats, and marine organisms with pelagic larval stages. While individuals located on either end of a species' distribution may exhibit clear genetic, phenotypic, and ecological differences, IBD produces subtle changes in allele frequencies across space, making it difficult to draw clear boundaries for conservation purposes in the absence of discrete population structure. Here, we highlight potential pitfalls that arise when applying common methods for delineating CUs to continuously distributed organisms and review existing methods for detecting subtle breakpoints in patterns of IBD that can indicate barriers to gene flow in highly mobile taxa. In addition, we propose a new framework for identifying CUs in all organisms, including those characterized by continuous genomic differentiation, and suggest several possible ways to harness the information contained in patterns of IBD to guide conservation and management decisions.

Clock-linked genes underlie seasonal migratory timing in a diurnal raptor.

Seasonal migration is a dynamic natural phenomenon that allows organisms to exploit favourable habitats across the annual cycle. While the morphological, physiological and behavioural changes associated with migratory behaviour are well characterized, the genetic basis of migration and its link to endogenous biological time-keeping pathways are poorly understood. Historically, genome-wide research has focused on genes of large effect, whereas many genes of small effect may work together to regulate complex traits like migratory behaviour. Here, we explicitly relax stringent outlier detection thresholds and, as a result, discover how multiple biological time-keeping genes are important to migratory timing in an iconic raptor species, the American kestrel (Falco sparverius). To validate the role of candidate loci in migratory timing, we genotyped kestrels captured across autumn migration and found significant associations between migratory timing and genetic variation in metabolic and light-input pathway genes that modulate biological clocks (top1, phlpp1, cpne4 and peak1). Further, we demonstrate that migrating individuals originated from a single panmictic source population, suggesting the existence of distinct early and late migratory genotypes (i.e. chronotypes). Overall, our results provide empirical support for the existence of a within-population-level polymorphism in genes underlying migratory timing in a diurnally migrating raptor.

Phylogenomic Data Reveal Widespread Introgression Across the Range of an Alpine and Arctic Specialist.

Understanding how gene flow affects population divergence and speciation remains challenging. Differentiating one evolutionary process from another can be difficult because multiple processes can produce similar patterns, and more than one process can occur simultaneously. Although simple population models produce predictable results, how these processes balance in taxa with patchy distributions and complicated natural histories is less certain. These types of populations might be highly connected through migration (gene flow), but can experience stronger effects of genetic drift and inbreeding, or localized selection. Although different signals can be difficult to separate, the application of high-throughput sequence data can provide the resolution necessary to distinguish many of these processes. We present whole-genome sequence data for an avian species group with an alpine and arctic tundra distribution to examine the role that different population genetic processes have played in their evolutionary history. Rosy-finches inhabit high elevation mountaintop sky islands and high-latitude island and continental tundra. They exhibit extensive plumage variation coupled with low levels of genetic variation. Additionally, the number of species within the complex is debated, making them excellent for studying the forces involved in the process of diversification, as well as an important species group in which to investigate species boundaries. Total genomic variation suggests a broadly continuous pattern of allele frequency changes across the mainland taxa of this group in North America. However, phylogenomic analyses recover multiple distinct, well supported, groups that coincide with previously described morphological variation and current species-level taxonomy. Tests of introgression using D-statistics and approximate Bayesian computation reveal significant levels of introgression between multiple North American taxa. These results provide insight into the balance between divergent and homogenizing population genetic processes and highlight remaining challenges in interpreting conflict between different types of analytical approaches with whole-genome sequence data. [ABBA-BABA; approximate Bayesian computation; gene flow; phylogenomics; speciation; whole-genome sequencing.].

A general theory of avian migratory connectivity.

Birds exhibit a remarkable array of seasonal migrations. Despite much research describing migratory behaviour, the underlying forces driving how a species' breeding and wintering populations redistribute each year, that is, migratory connectivity, remain largely unknown. Here, we test the hypothesis that birds migrate in a way that minimises energy expenditure while considering intraspecific competition for energy acquisition, by developing a modelling framework that simulates an optimal redistribution of individuals between breeding and wintering areas. Using 25 species across the Americas, we find that the model accurately predicts empirical migration patterns, and thus offers a general explanation for migratory connectivity based on first ecological and energetic principles. Our model provides a strong basis for exploring additional processes underlying the ecology and evolution of migration, but also a framework for predicting how migration impacts local adaptation across seasons and how environmental change may affect population dynamics in migratory species.

Genetic variation reveals individual-level climate tracking across the annual cycle of a migratory bird.

For migratory species, seasonal movements complicate local climate adaptation, as it is unclear whether individuals track climate niches across the annual cycle. In the migratory songbird yellow warbler (Setophaga petechia), we find a correlation between individual-level wintering and breeding precipitation, but not temperature. Birds wintering in the driest regions of the Neotropics breed in the driest regions of North America. Individuals from drier regions also possess distinct morphologies and population responses to varying rainfall. We find a positive association between bill size and breeding season precipitation which, given documented climate-associated genomic variation, might reflect adaptation to local precipitation regimes. Relative abundance in the breeding range is linked to interannual fluctuations in precipitation, but the directionality of this response varies across geography. Together, our results suggest that variation in climate optima may exist across the breeding range of yellow warblers and provide a mechanism for selection across the annual cycle.

An island-hopping bird reveals how founder events shape genome-wide divergence.

When populations colonize new areas, both strong selection and strong drift can be experienced due to novel environments and small founding populations, respectively. Empirical studies have predominantly focused on the phenotype when assessing the role of selection, and limited neutral-loci when assessing founder-induced loss of diversity. Consequently, the extent to which processes interact to influence evolutionary trajectories is difficult to assess. Genomic-level approaches provide the opportunity to simultaneously consider these processes. Here, we examine the roles of selection and drift in shaping genomic diversity and divergence in historically documented sequential island colonizations by the silvereye (Zosterops lateralis). We provide the first empirical demonstration of the rapid appearance of highly diverged genomic regions following population founding, the position of which are highly idiosyncratic. As these regions rarely contained loci putatively under selection, it is most likely that these differences arise via the stochastic nature of the founding process. However, selection is required to explain rapid evolution of larger body size in insular silvereyes. Reconciling our genomic data with these phenotypic patterns suggests there may be many genomic routes to the island phenotype, which vary across populations. Finally, we show that accelerated divergence associated with multiple founding steps is the product of genome-wide rather than localized differences, and that diversity erodes due to loss of rare alleles. However, even multiple founder events do not result in divergence and diversity levels seen in evolutionary older subspecies, and therefore do not provide a shortcut to speciation as proposed by founder-effect speciation models.

Linking climate niches across seasons to assess population vulnerability in a migratory bird.

Global loss of biodiversity has placed new urgency on the need to understand factors regulating species response to rapid environmental change. While specialists are often less resilient to rapid environmental change than generalists, species-level analyses may obscure the extent of specialization when locally adapted populations vary in climate tolerances. Until recently, quantification of the degree of climate specialization in migratory birds below the species level was hindered by a lack of genomic and tracking information, but recent technological advances have helped to overcome these barriers. Here we take a genome-wide genetic approach to mapping population-specific migratory routes and quantifying niche breadth within genetically distinct populations of a migratory bird, the willow flycatcher (Empidonax traillii), which exhibits variation in the severity of population declines across its breeding range. While our sample size is restricted to the number of genetically distinct populations within the species, our results support the idea that locally adapted populations of the willow flycatcher with narrow climatic niches across seasons are already federally listed as endangered or in steep decline, while populations with broader climatic niches have remained stable in recent decades. Overall, this work highlights the value of quantifying niche breadth within genetically distinct groups across time and space when attempting to understand the factors that facilitate or constrain the response of locally adapted populations to rapid environmental change.

Precipitation and vegetation shape patterns of genomic and craniometric variation in the central African rodent Praomys misonnei.

Predicting species' capacity to respond to climate change is an essential first step in developing effective conservation strategies. However, conservation prioritization schemes rarely take evolutionary potential into account. Ecotones provide important opportunities for diversifying selection and may thus constitute reservoirs of standing variation, increasing the capacity for future adaptation. Here, we map patterns of environmentally associated genomic and craniometric variation in the central African rodent Praomys misonnei to identify areas with the greatest turnover in genomic composition. We also project patterns of environmentally associated genomic variation under future climate change scenarios to determine where populations may be under the greatest pressure to adapt. While precipitation gradients influence both genomic and craniometric variation, vegetation structure is also an important determinant of craniometric variation. Areas of elevated environmentally associated genomic and craniometric variation overlap with zones of rapid ecological transition underlining their importance as reservoirs of evolutionary potential. We also find that populations in the Sanaga river basin, central Cameroon and coastal Gabon are likely to be under the greatest pressure from climate change. Lastly, we make specific conservation recommendations on how to protect zones of high evolutionary potential and identify areas where populations may be the most susceptible to climate change.

Rapid morphological divergence following a human-mediated introduction: the role of drift and directional selection.

Theory predicts that when populations are established by few individuals, random founder effects can facilitate rapid phenotypic divergence even in the absence of selective processes. However, empirical evidence from historically documented colonisations suggest that, in most cases, drift alone is not sufficient to explain the rate of morphological divergence. Here, using the human-mediated introduction of the silvereye (Zosterops lateralis) to French Polynesia, which represents a potentially extreme example of population founding, we reassess the potential for morphological shifts to arise via drift alone. Despite only 80 years of separation from their New Zealand ancestors, French Polynesian silvereyes displayed significant changes in body and bill size and shape, most of which could be accounted for by drift, without the need to invoke selection. However, signatures of selection at genes previously identified as candidates for bill size and body shape differences in a range of bird species, also suggests a role for selective processes in driving morphological shifts within this population. Twenty-four SNPs in our RAD-Seq dataset were also found to be strongly associated with phenotypic variation. Hence, even under population founding extremes, when it is difficult to reject drift as the sole mechanism based on rate tests of phenotypic shifts, the additional role of divergent natural selection in novel environments can be revealed at the level of the genome.

A genoscape-network model for conservation prioritization in a migratory bird.

Migratory animals are declining worldwide and coordinated conservation efforts are needed to reverse current trends. We devised a novel genoscape-network model that combines genetic analyses with species distribution modeling and demographic data to overcome challenges with conceptualizing alternative risk factors in migratory species across their full annual cycle. We applied our method to the long distance, Neotropical migratory bird, Wilson's Warbler (Cardellina pusilla). Despite a lack of data from some wintering locations, we demonstrated how the results can be used to help prioritize conservation of breeding and wintering areas. For example, we showed that when genetic, demographic, and network modeling results were considered together it became clear that conservation recommendations will differ depending on whether the goal is to preserve unique genetic lineages or the largest number of birds per unit area. More specifically, if preservation of genetic lineages is the goal, then limited resources should be focused on preserving habitat in the California Sierra, Basin Rockies, or Coastal California, where the 3 most vulnerable genetic lineages breed, or in western Mexico, where 2 of the 3 most vulnerable lineages overwinter. Alternatively, if preservation of the largest number of individuals per unit area is the goal, then limited conservation dollars should be placed in the Pacific Northwest or Central America, where densities are estimated to be the highest. Overall, our results demonstrated the utility of adopting a genetically based network model for integrating multiple types of data across vast geographic scales and better inform conservation decision-making for migratory animals.

Un Modelo de Redes de Panorama Poblacional para la Priorización de la Conservación de un Ave Migratoria Resumen Los animales migratorios están pasando por una declinación mundial y se requieren esfuerzos coordinados de conservación para revertir las tendencias actuales. Diseñamos un modelo novedoso de redes de panorama poblacional que combina el análisis genético con el modelado de la distribución de especies y los datos demográficos para sobreponerse a los obstáculos con la conceptualización de los factores alternativos de riesgo en las especies migratorias durante su ciclo anual completo. Aplicamos nuestro método al chipe de corona negra (Cardellina pusilla), un ave migratoria neotropical que recorre largas distancias. A pesar de la falta de datos de algunas localidades de invernación, mostramos cómo pueden usarse los resultados para ayudar a priorizar la conservación de las áreas de reproducción y de invernación. Por ejemplo, mostramos que cuando se consideraron en conjunto los resultados del modelado genético, demográfico y de redes queda claro que las recomendaciones de conservación diferirán dependiendo de si el objetivo es preservar linajes genéticos únicos o el mayor número de aves por unidad de área. Más específicamente, si el objetivo es la conservación de los linajes genéticos, entonces los recursos limitados deberían enfocarse en preservar el hábitat en la Sierra de California, la Cuenca de las Rocallosas, la costa de California (lugares en donde se reproducen los tres linajes genéticos más vulnerables) o en el oeste de México (en donde dos de los tres linajes más vulnerables pasan el invierno). Alternativamente, si el objetivo es la conservación del mayor número de individuos por unidad de área, entonces el financiamiento limitado debería aplicarse en el noroeste del Pacífico o en América Central, en donde se estima que las densidades poblacionales son las más altas. En general, nuestros resultados demostraron la utilidad de adoptar un modelo de redes basadas en la genética para la integración de datos a lo largo de escalas geográficas amplias y para informar de mejor manera la toma de decisiones de conservación para los animales migratorios.

Ecological genomics predicts climate vulnerability in an endangered southwestern songbird.

Few regions have been more severely impacted by climate change in the USA than the Desert Southwest. Here, we use ecological genomics to assess the potential for adaptation to rising global temperatures in a widespread songbird, the willow flycatcher (Empidonax traillii), and find the endangered desert southwestern subspecies (E. t. extimus) most vulnerable to future climate change. Highly significant correlations between present abundance and estimates of genomic vulnerability - the mismatch between current and predicted future genotype-environment relationships - indicate small, fragmented populations of the southwestern willow flycatcher will have to adapt most to keep pace with climate change. Links between climate-associated genotypes and genes important to thermal tolerance in birds provide a potential mechanism for adaptation to temperature extremes. Our results demonstrate that the incorporation of genotype-environment relationships into landscape-scale models of climate vulnerability can facilitate more precise predictions of climate impacts and help guide conservation in threatened and endangered groups.

Genomic islands of divergence or opportunities for introgression?

In animals, introgression between species is often perceived as the breakdown of reproductive isolating mechanisms, but gene flow between incipient species can also represent a source for potentially beneficial alleles. Recently, genome-wide datasets have revealed clusters of differentiated loci ('genomic islands of divergence') that are thought to play a role in reproductive isolation and therefore have reduced gene flow. We use simulations to further examine the evolutionary forces that shape and maintain genomic islands of divergence between two subspecies of the migratory songbird, Swainson's thrush (Catharus ustulatus), which have come into secondary contact since the last glacial maximum. We find that, contrary to expectation, gene flow is high within islands and is highly asymmetric. In addition, patterns of nucleotide diversity at highly differentiated loci suggest selection was more frequent in a single ecotype. We propose a mechanism whereby beneficial alleles spread via selective sweeps following a post-glacial demographic expansion in one subspecies and move preferentially across the hybrid zone. We find no evidence that genomic islands are the result of divergent selection or reproductive isolation, rather our results suggest that differentiated loci both within and outside islands could provide opportunities for adaptive introgression across porous species boundaries.

Genomic divergence across ecological gradients in the Central African rainforest songbird (Andropadus virens).

The little greenbul, a common rainforest passerine from sub-Saharan Africa, has been the subject of long-term evolutionary studies to understand the mechanisms leading to rainforest speciation. Previous research found morphological and behavioural divergence across rainforest-savannah transition zones (ecotones), and a pattern of divergence with gene flow suggesting divergent natural selection has contributed to adaptive divergence and ecotones could be important areas for rainforests speciation. Recent advances in genomics and environmental modelling make it possible to examine patterns of genetic divergence in a more comprehensive fashion. To assess the extent to which natural selection may drive patterns of differentiation, here we investigate patterns of genomic differentiation among populations across environmental gradients and regions. We find compelling evidence that individuals form discrete genetic clusters corresponding to distinctive environmental characteristics and habitat types. Pairwise FST between populations in different habitats is significantly higher than within habitats, and this differentiation is greater than what is expected from geographic distance alone. Moreover, we identified 140 SNPs that showed extreme differentiation among populations through a genomewide selection scan. These outliers were significantly enriched in exonic and coding regions, suggesting their functional importance. Environmental association analysis of SNP variation indicates that several environmental variables, including temperature and elevation, play important roles in driving the pattern of genomic diversification. Results lend important new genomic evidence for environmental gradients being important in population differentiation.

A role for migration-linked genes and genomic islands in divergence of a songbird.

Next-generation sequencing has made it possible to begin asking questions about the process of divergence at the level of the genome. For example, recently, there has been a debate around the role of 'genomic islands of divergence' (i.e. blocks of outlier loci) in facilitating the process of speciation-with-gene-flow. The Swainson's thrush, Catharus ustulatus, is a migratory songbird with two genetically distinct subspecies that differ in a number of traits known to be involved in reproductive isolation in birds (plumage coloration, song and migratory behaviour), despite contemporary gene flow along a secondary contact zone. Here, we use RAD-PE sequencing to test emerging hypotheses about the process of divergence at the level of the genome and identify genes and gene regions involved in differentiation in this migratory songbird. Our analyses revealed distinct genomic islands on 15 of the 23 chromosomes and an accelerated rate of divergence on the Z chromosome, one of the avian sex chromosomes. Further, an analysis of loci linked to traits known to be involved in reproductive isolation in songbirds showed that genes linked to migration are significantly more differentiated than expected by chance, but that these genes lie primarily outside the genomic islands. Overall, our analysis supports the idea that genes linked to migration play an important role in divergence in migratory songbirds, but we find no compelling evidence that the observed genomic islands are facilitating adaptive divergence in migratory behaviour.