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Structural variants (SVs) are a major source of genetic variation, but accurate descriptions in natural populations and connections with phenotypic traits remain scarce. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (i) characterized the genome-wide distribution, frequency and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (ii) used these SVs to study the genetics of seasonal migration. We detected >15K 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 these SVs 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 one trait – direction – and one 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.

Bird migration is one of the most amazing biological phenomena exhibited by organisms today, with birds as small as three grams travelling thousands of kilometers twice each year. Most people are familiar with this behaviour; they likely recognize the seasonal movements of birds each year and may have even witnessed specific migratory events (e.g., geese flying in their characteristic V-formations). What many people may not know is that bird migration has a strong genetic basis, especially in groups like songbirds who migrate alone and at night, preventing juveniles from following more experienced adult birds on their first migration. Successful migration also requires the coordinated function of many traits, not only behavioural traits like timing and orientation but also morphological and physiological traits to permit these long distance treks. Together, these traits comprise what has been called the 'migratory syndrome'. In this primer, we provide a broad overview of research on the genetics of migratory traits, from early experimental work to future functional assays and their importance for bird conservation. We focus primarily on songbirds as most work on the genetics of migration has been conducted with this group.

Hybridization has important effects on the evolutionary trajectories of natural populations but estimates of this process in the wild and at the individual-level are lacking. Justyn et al. attempted to fill this gap using the citizen science database eBird but there are limitations to this approach. Here, we outline and directly test these limitations using literature searches, case studies, and a comparison between eBird and Birds of North America (BNA), a database that documents hybridization using the scientific literature. We use a hybrid zone between Lazuli and Indigo buntings to highlight the importance of considering geographic range when estimating rates of hybridization and two literature searches to show the importance of considering cryptic hybrids (those that cannot be identified using phenotypic traits) when quantifying these rates. We also use BNA and a case study of hybrid White-faced and Glossy Ibises to show that citizen scientists are underreporting hybrids compared with experts. Justyn et al. highlighted an important gap in the literature, but their results likely represent the lower limit of hybridization between birds and a more nuanced interpretation of their results (e.g., considering extrinsic postzygotic selection) is needed.

Closely related populations often display similar patterns of genomic differentiation, yet it remains an open question which ecological and evolutionary forces generate these patterns. The leading hypothesis is that this similarity in divergence is driven by parallel natural selection. However, several recent studies have suggested that these patterns may instead be a product of the depletion of genetic variation that occurs as result of background selection (i.e., linked negative selection). To date, there have been few direct tests of these competing hypotheses. To determine the relative contributions of background selection and parallel selection to patterns of repeated differentiation, we examined 24 independently derived populations of freshwater stickleback occupying a variety of niches and estimated genomic patterns of differentiation in each relative to their common marine ancestor. Patterns of genetic differentiation were strongly correlated across pairs of freshwater populations adapting to the same ecological niche, supporting a role for parallel natural selection. In contrast to other recent work, our study comparing populations adapting to the same niche produced no evidence signifying that similar patterns of genomic differentiation are generated by background selection. We also found that overall patterns of genetic differentiation were considerably more similar for populations found in closer geographic proximity. In fact, the effect of geography on the repeatability of differentiation was greater than that of parallel selection. Our results suggest that shared selective landscapes and ancestral variation are the key drivers of repeated patterns of differentiation in systems that have recently colonized novel environments.

Hybrid zones are particularly valuable for understanding the evolution of partial reproductive isolation between differentiated populations. An increasing number of hybrid zones have been inferred to move over time, but in most such cases zone movement has not been tested with long-term genomic data. The hybrid zone between Townsend's Warblers (Setophaga townsendi) and Hermit Warblers (S. occidentalis) in the Washington Cascades was previously inferred to be moving from northern S. townsendi southwards towards S. occidentalis, based on plumage and behavioural patterns as well as a 2000-km genetic wake of hermit mitochondrial DNA (mtDNA) in coastal Townsend's Warblers. We directly tested whether hybrid zone position has changed over 2-3 decades by tracking plumage, mtDNA and nuclear genomic variation across the hybrid zone over two sampling periods (1987-94 and 2015-16). Surprisingly, there was no significant movement in genomic or plumage cline centres between the two time periods. Plumage cline widths were narrower than expected by neutral diffusion, consistent with a 'tension zone' model, in which selection against hybrids is balanced by movement of parental forms into the zone. Our results indicate that this hybrid zone is either stable in its location or moving at a rate that is not detectable over 2-3 decades. Despite considerable gene flow, the stable clines in multiple phenotypic and genotypic characters over decades suggest evolutionary stability of this young pair of sister species, allowing divergence to continue. We propose a novel biogeographic scenario to explain these patterns: rather than the hybrid zone having moved thousands of kilometres to its current position, inland Townsend's met coastal Hermit Warbler populations along a broad front of the British Columbia and Alaska coast and hybridization led to replacement of the Hermit Warbler plumage with Townsend's Warbler plumage patterns along this coastline. Hence, hybrid zones along British Columbia and Alaska moved only a short distance from the inland to the coast, whereas the Hermit Warbler phenotype appears stable in Washington and further south. This case provides an example of the complex biogeographic processes that have led to the distribution of current phenotypes within and among closely related species.

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1–4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic and molecular diversity, by analysing 363 genomes from 92.4% of bird families—including 267 newly sequenced genomes produced for phase II of the Bird 10,000 Genomes (B10K) Project. We use this comparative genome dataset in combination with a pipeline that leverages a reference-free whole-genome alignment to identify orthologous regions in greater numbers than has previously been possible and to recognize genomic novelties in particular bird lineages. The densely sampled alignment provides a single-base-pair map of selection, has more than doubled the fraction of bases that are confidently predicted to be under conservation and reveals extensive patterns of weak selection in predominantly non-coding DNA. Our results demonstrate that increasing the diversity of genomes used in comparative studies can reveal more shared and lineage-specific variation, and improve the investigation of genomic characteristics. We anticipate that this genomic resource will offer new perspectives on evolutionary processes in cross-species comparative analyses and assist in efforts to conserve species., A dataset of the genomes of 363 species from the Bird 10,000 Genomes Project shows increased power to detect shared and lineage-specific variation, demonstrating the importance of phylogenetically diverse taxon sampling in whole-genome sequencing.

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.

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., eLife digest 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.

Birds are one of the most recognizable and diverse groups of organisms on earth. This group has played an important role in many fields, including the development of methods in behavioral ecology and evolutionary theory. The use of population genomics took off following the advent of high-throughput sequencing in various taxa. Several features of avian genomes make them particularly amenable for work in this field, including their nucleated red blood cells permitting easy DNA extraction and small, compact genomes. We review the latest findings in the population genomics of birds here, emphasizing questions related to behavior, ecology, evolution, and conservation. Additionally, we include insights in trait mapping and the ability to obtain accurate estimates of important summary statistics for conservation (e.g., genetic diversity and inbreeding). We highlight roadblocks that will need to be overcome in order to advance work on the population genomics of birds and prospects for future work. Roadblocks include the assembly of more contiguous reference genomes using long-reads and optical mapping. Prospects include the integration of population genomics with additional fields (e.g., landscape genetics, phylogeography, and genomic mapping) along with studies beyond genetic variants (e.g., epigenetics).

Birds are one of the most recognizable and diverse groups of organisms on earth. This group has played an important role in many fields, including the development of methods in behavioral ecology and evolutionary theory. The use of population genomics took off following the advent of high-throughput sequencing in various taxa. Several features of avian genomes make them particularly amenable for work in this field, including their nucleated red blood cells permitting easy DNA extraction and small, compact genomes. We review the latest findings in the population genomics of birds here, emphasizing questions related to behavior, ecology, evolution, and conservation. Additionally, we include insights in trait mapping and the ability to obtain accurate estimates of important summary statistics for conservation (e.g., genetic diversity and inbreeding). We highlight roadblocks that will need to be overcome in order to advance work on the population genomics of birds and prospects for future work. Roadblocks include the assembly of more contiguous reference genomes using long-reads and optical mapping. Prospects include the integration of population genomics with additional fields (e.g., landscape genetics, phylogeography, and genomic mapping) along with studies beyond genetic variants (e.g., epigenetics).

In Supplementary Table 1 of this Article, 23 samples (B10K-DU-029-32, B10K-DU-029-33, B10K-DU-029-36 to B10K-DU-029-44, B10K-DU- 029-46, B10K-DU-029-47, B10K-DU-029-49 to B10K-DU-029-53, B10K-DU- 029-75 to B10K-DU-029-77, B10K-DU-029-80, and B10K-DU-030-03; styled in boldface in the revised table) were assigned to the incorrect institution. Supplementary Table 1 has been amended to reflect the correct source institution for these samples, and associated data (tissue, museum ID/source specimen ID, site, state/province, latitude, longitude, date collected and sex) have been updated accordingly. The original table is provided as Supplementary Information to this Amendment, and the original Article has been corrected online.

Details on the genetics of behavioral and quantitative phenotypes remain limited to a few organisms. Such information is central to understanding both adaptation and speciation, as many of these phenotypes reduce gene flow between taxa [1–3]. Hybrid zones provide an ideal arena for studying this topic, as they consist of recombinant genotypes that allow genetic mapping of traits distinguishing natural populations [4]. We examined the genetic basis of migratory orientation and plumage color, both of which may contribute to speciation, in a hybrid zone between two groups of Swainson's thrushes that differ in these traits. We identified a cluster of SNPs on chromosome 4 strongly associated with migratory orientation. Genes involved with the circadian clock, nervous system, and cell signaling were located here and included candidates implicated in smaller-scale studies of migration in different animal groups, supporting previous suggestions that there is a common gene package for migration [5]. Plumage color was more polygenic than migratory orientation but showed strong associations on the Z chromosome that included SNPs linked to TYRP1, a gene involved in the production of eumelanin. We integrated these results with genomic data from pure populations and found that regions associated with both phenotypes co-localized with regions of elevated relative differentiation between the groups. This finding relates to the literature on islands of differentiation [6–8] by implicating divergent selection in generating these peaks. Together, our results identify specific genomic regions involved in both the regulation of complex phenotypes across animal groups and speciation [9]. © 2016 Elsevier Ltd

Detailed evaluations of genomic variation between sister species often reveal distinct chromosomal regions of high relative differentiation (i.e., “islands of differentiation” in F), but there is much debate regarding the causes of this pattern. We briefly review the prominent models of genomic islands of differentiation and compare patterns of genomic differentiation in three closely related pairs of New World warblers with the goal of evaluating support for the four models. Each pair (MacGillivray's/mourning warblers; Townsend's/black-throated green warblers; and Audubon's/myrtle warblers) consists of forms that were likely separated in western and eastern North American refugia during cycles of Pleistocene glaciations and have now come into contact in western Canada, where each forms a narrow hybrid zone. We show strong differences between pairs in their patterns of genomic heterogeneity in F, suggesting differing selective forces and/or differing genomic responses to similar selective forces among the three pairs. Across most of the genome, levels of within-group nucleotide diversity (π) are almost as large as levels of between-group nucleotide distance (π) within each pair, suggesting recent common ancestry and/or gene flow. In two pairs, a pattern of the F peaks having low π suggests that selective sweeps spread between geographically differentiated groups, followed by local differentiation. This “sweep-before-differentiation” model is consistent with signatures of gene flow within the yellow-rumped warbler species complex. These findings add to our growing understanding of speciation as a complex process that can involve phases of adaptive introgression among partially differentiated populations., Major research funding was provided by the Natural Sciences and Engineering Research Council of Canada (Discovery Grant 311931 to DEI).

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 re-estimated 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 forFSTand 26% fordXY), supporting a role for processes at conserved genomic features in generating heterogeneous patterns of differentiation. This suggestion was reinforced by linear models identifying several genomic features (e.g., gene densities) as significant predictors ofFSTanddXYrepeatability.FSTrepeatability was higher among pairs that were further along the speciation continuum (i.e., more reproductively isolated), suggesting that early stages of speciation may be dominated by positive selection that is different between pairs and replaced by processes acting according to shared genomic features as speciation proceeds.

Endogenous selection is often implicated in the maintenance of stability of natural hybrid zones. Environmental conditions often vary across these zones, suggesting that local adaptation to ecological conditions could also play a role in this process. We used niche modeling to investigate these alternatives in a hybrid zone between two species of brown lemur (Eulemur rufifrons and E. cinereiceps) in southeastern Madagascar. We produced ecological niche models (ENMs) for parental and hybrid populations and compared values of niche overlap to null expectations using identity and background tests. All three taxonomic groups had nonequivalent ENMs with limited spatial overlap, supporting a role for niche divergence and local adaptation in the maintenance of this zone. However, values of niche overlap between ENMs were not greater than null expectations controlling for background environmental differences. These results could suggest that taxa in this hybrid zone inhabit portions of their environments that are more similar to their backgrounds, i.e., niche conservatism. Nevertheless, we did find evidence of niche divergence when using background tests that examined environmental variables separately. Although we could not rule out models indicating selection against hybrids, most lines of evidence were consistent with predictions for the bounded superiority model of hybrid zone stability. This study thus provides support that exogenous, environmental selection may be responsible for maintaining the hybrid zone, and may be implicated in the evolutionary divergence of these taxa.

Summary Selecting breeding habitats that ameliorate environmental limits on fitness and facilitate successful reproduction should benefit individual animals. This is particularly true in the temperate zone, where breeding early in a season presents a unique series of environmental challenges that can limit an individual's fitness. While many studies document links between habitat quality and reproductive success, few identify the cues used to assess habitat quality or the components of reproduction most influenced by occupying higher quality habitat, particularly during the early breeding season. We used detailed spatial maps and observations of all early season nesting attempts in an insular song sparrow (Melospiza melodia) population over 38 years to estimate the influence of nest-site preference on reproductive success and to test whether relative microclimate or food availability may act as cues for early season site selection. Female sparrows in preferred early season nest sites had earlier laying dates, exhibited more energetically efficient incubation behaviour and produced more offspring that recruited to the population than those nesting in less-preferred sites. Preference for potential nesting sites was positively related to leaf damage by Lepidopteran larvae, an indicator of food abundance, negatively related to early season microclimate, likely due to greater vegetation cover, and unrelated to site-specific plant phenology. Our findings show that breeding in preferred, high-quality habitat may offer females a fitness advantage by facilitating early laying and the production of offspring more likely to recruit to the population at a lower potential reproductive cost to the parent. We provide a clear demonstration of potential links between habitat preference and quality and their contributions to the ecology and life history of animals in seasonal environments.

Differential gene flow, reductions in diversity following linked selection and/or features of the genome can structure patterns of genomic differentiation during the process of speciation. Possible sources of reproductive isolation are well studied between coastal and inland subspecies groups of Swainson's thrushes, with differences in seasonal migratory behaviour likely playing a key role in reducing hybrid fitness. We assembled and annotated a draft reference genome for this species and generated whole-genome shotgun sequence data for populations adjacent to the hybrid zone between these groups. We documented substantial genomewide heterogeneity in relative estimates of genetic differentiation between the groups. Within population diversity was lower in areas of high relative differentiation, supporting a role for selective sweeps in generating this pattern. Absolute genetic differentiation was reduced in these areas, further suggesting that recurrent selective sweeps in the ancestral population and/or between divergent populations following secondary contact likely occurred. Relative genetic differentiation was also higher near centromeres and on the Z chromosome, suggesting that features of the genome also contribute to genomewide heterogeneity. Genes linked to migratory traits were concentrated in islands of differentiation, supporting previous suggestions that seasonal migration is under divergent selection between Swainson's thrushes. Differences in migratory behaviour likely play a central role in the speciation of many taxa; we developed the infrastructure here to permit future investigations into the role several candidate genes play in reducing gene flow between not only Swainson's thrushes but other species as well.

Seasonal migration is the yearly long-distance movement of individuals between their breeding and wintering grounds. Individuals from nearly every animal group exhibit this behavior, but probably the most iconic migration is carried out by birds, from the classic V-shape formation of geese on migration to the amazing nonstop long-distance flights undertaken by Arctic Terns Sterna paradisaea. In this chapter, we discuss how seasonal migration has shaped the field of evolution. First, this behavior is known to turn on and off quite rapidly, but controversy remains concerning where this behavior first evolved geographically and whether the ancestral state was sedentary or migratory (Fig. 7.1d, e). We review recent work using new analytical techniques to provide insight into this topic. Second, it is widely accepted that there is a large genetic basis to this trait, especially in groups like songbirds that migrate alone and at night precluding any opportunity for learning. Key hypotheses on this topic include shared genetic variation used by different populations to migrate and only few genes being involved in its control. We summarize recent work using new techniques for both phenotype and genotype characterization to evaluate and challenge these hypotheses. Finally, one topic that has received less attention is the role these differences in migratory phenotype could play in the process of speciation. Specifically, many populations breed next to one another but take drastically different routes on migration (Fig. 7.2). This difference could play an important role in reducing gene flow between populations, but our inability to track most birds on migration has so far precluded evaluations of this hypothesis. The advent of new tracking techniques means we can track many more birds with increasing accuracy on migration, and this work has provided important insight into migration's role in speciation that we will review here.

Studies of hybrid zones can inform our understanding of reproductive isolation and speciation. Two species of brown lemur (Eulemur rufifrons and E. cinereiceps) form an apparently stable hybrid zone in the Andringitra region of south-eastern Madagascar. The aim of this study was to identify factors that contribute to this stability. We sampled animals at 11 sites along a 90-km transect through the hybrid zone and examined variation in 26 microsatellites, the D-loop region of mitochondrial DNA, six pelage and nine morphological traits; we also included samples collected in more distant allopatric sites. Clines in these traits were noncoincident, and there was no increase in either inbreeding coefficients or linkage disequilibrium at the centre of the zone. These results could suggest that the hybrid zone is maintained by weak selection against hybrids, conforming to either the tension zone or geographical selection-gradient model. However, a closer examination of clines in pelage and microsatellites indicates that these clines are not sigmoid or stepped in shape but instead plateau at their centre. Sites within the hybrid zone also occur in a distinct habitat, characterized by greater seasonality in precipitation and lower seasonality in temperature. Together, these findings suggest that the hybrid zone may follow the bounded superiority model, with exogenous selection favouring hybrids within the transitional zone. These findings are noteworthy, as examples supporting the bounded superiority model are rare and may indicate a process of ecologically driven speciation without geographical isolation.

Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (FST and dXY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination. © 2017 John Wiley & Sons Ltd

Migratory traits in birds have been shown to have a strong heritable component and several candidate genes have been suggested to control these migratory traits. To investigate if the genetic makeup of one or a set of these candidate genes can be used to identify a general pattern between migratory and non-migratory birds, we extracted genomic sequence data for 25 hypothesised candidate genes for migration from 70 available genomes across all orders of Aves and characterised sequence divergence between migratory and non-migratory phenotypes. When examining each gene separately across all species, we did not identify any genetic variants in candidate genes that distinguished migrants from non-migrants; any resulting pattern was driven by the phylogenetic signal. This was true for each gene analysed independently, but also for concatenated sequence alignments of all candidate genes combined. We also attempted to distinguish between migrant and non-migrants using structural features at four candidate genes that have previously been reported to show associated with migratory behaviour but did not pick up a signal for migratory phenotype here either. Finally, a screen for dN/dS ratio across all focal candidate genes to probe for putative features of selection did not uncover a pattern, though this might not be expected given the broad phylogenetic scale used here. Our study demonstrates the potential of public genomic data to test for general patterns of migratory gene candidates in a cross-species comparative context, and raise questions on the applicability of candidate gene approaches in a macro-evolutionary context to understand the genetic architecture of migratory behaviour. Electronic supplementary material The online version of this article (doi:10.1007/s00359-017-1184-6) contains supplementary material, which is available to authorized users.

Recent technological developments allow investigation of the repeatability of evolution at the genomic level. Such investigation is particularly powerful when applied to a ring species, in which spatial variation represents changes during the evolution of two species from one. We examined genomic variation among three subspecies of the greenish warbler ring species, using genotypes at 13 013 950 nucleotide sites along a new greenish warbler consensus genome assembly. Genomic regions of low within-group variation are remarkably consistent between the three populations. These regions show high relative differentiation but low absolute differentiation between populations. Comparisons with outgroup species show the locations of these peaks of relative differentiation are not well explained by phylogenetically conserved variation in recombination rates or selection. These patterns are consistent with a model in which selection in an ancestral form has reduced variation at some parts of the genome, and those same regions experience recurrent selection that subsequently reduces variation within each subspecies. The degree of heterogeneity in nucleotide diversity is greater than explained by models of background selection, but is consistent with selective sweeps. Given the evidence that greenish warblers have had both population differentiation for a long period of time and periods of gene flow between those populations, we propose that some genomic regions underwent selective sweeps over a broad geographic area followed by within-population selection-induced reductions in variation. An important implication of this ‘sweep-before-differentiation’ model is that genomic regions of high relative differentiation may have moved among populations more recently than other genomic regions. © 2016 John Wiley Sons Ltd

Recent technological developments allow investigation of the repeatability of evolution at the genomic level. Such investigation is particularly powerful when applied to a ring species, in which spatial variation represents changes during the evolution of two species from one. We examined genomic variation among three subspecies of the greenish warbler ring species, using genotypes at 13,013,950 nucleotide sites along a new greenish warbler consensus genome assembly. Genomic regions of low within-group variation are remarkably consistent between the three populations. These regions show high relative differentiation but low absolute differentiation between populations. Comparisons with outgroup species show the locations of these peaks of relative differentiation are not well explained by phylogenetically-conserved variation in recombination rates or selection. These patterns are consistent with a model in which selection in an ancestral form has reduced variation at some parts of the genome, and those same regions experience recurrent selection that subsequently reduces variation within each subspecies. The degree of heterogeneity in nucleotide diversity is greater than explained by models background selection, but are consistent with selective sweeps. Given the evidence that greenish warblers have had both population differentiation for a long period of time and periods of gene flow between those populations, we propose that some genomic regions underwent selective sweeps over a broad geographic area followed by within-population selection-induced reductions in variation. An important implication of this “sweep-before-differentiation” model is that genomic regions of high relative differentiation may have moved among populations more recently than other genomic regions.

Knowledge of both population size and genetic diversity is critical for assessing extinction risk but few studies include concurrent estimates of these two components of population biology. We conducted an investigation of population density and size, and genetic variation and past demographic events, of the Endangered grey-headed lemurEulemur cinereicepsin south-east Madagascar. We estimated lemur density using line-transect surveys and used satellite imagery to calculate forest fragment area in three localities. We collected tissue samples from 53 individuals and used 26 polymorphic microsatellite loci to obtain measures of population structure (divergence and diversity) across these localities. We tested the probability of past bottleneck events using three models. Contrary to expectation, there were no significant differences in population density across localities. Genetic diversity decreased, but not significantly, with decreasing habitat area and population size. We found a higher likelihood of past bottleneck events in the fragmented coastal populations. The low population size and prior decline in diversity in coastal patches are consistent with their isolation, anthropogenic disturbance, and exposure to cyclone activity. The similarities in the estimates of density between continuous and fragmented sites may indicate recent population growth in the fragments but these populations nevertheless remain at risk from reduced levels of genetic variation. These patterns should be confirmed with more extensive sampling across the limited range ofE. cinereiceps.

Frequent copulation is assumed to be an important male reproductive strategy for paternity assurance in species with female sexual promiscuity. However, the empirical evidence supporting this hypothesis is limited. We examined copulation behaviour in relation to within-pair paternity in the socially monogamous tree swallow, Tachycineta bicolor, a passerine bird species with frequent copulation, a lack of mate guarding and high levels of extrapair paternity. We found that the frequency of within-pair copulation attempts increased and peaked just before the appearance of the first egg. A marked drop in the frequency of copulation attempts was observed once the first egg was laid. Furthermore, the frequency of successful within-pair copulations was highly repeatable for particular pairs within the 3 days prior to appearance of the first egg. Finally, males that obtained a higher number of successful within-pair copulations during this time also sired a larger proportion of the offspring in their own brood. Our findings suggest that frequent copulations just before the start of egg laying is an adaptation to decrease the risk of being cuckolded in the presence of sperm competition, and thus provide empirical support for the paternity assurance hypothesis. Crown Copyright 2008 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour. All rights reserved. Paternity assurance is critical to male fitness, particularly in species in which females frequently participate in extrapair copulations (EPCs) and males provide costly parental care. In response to fitness loss due to cuckoldry, several types of paternity assurance behaviour have evolved across taxa. One strategy is constant mate guarding by following, as males can protect their paternity by ensuring that no other male has an opportunity to mate with their paired female (Moller & Birkhead 1991). However, for some species, constant mate guarding may be constrained by territory protection or other activities. The paternity assurance hypothesis (Moller 1987; Simmons 1990), also known as the paternity confidence hypothesis (Eens & Pinxten 1995) and the sperm competition hypothesis (Birkhead et al. 1987), suggests that for species in which EPCs are common, males copulate frequently with their pair females to avoid being cuckolded. Males may minimize cuckoldry through frequent copulation by devaluing EPCs that their mates

The white-collared lemur (Eulemur cinereiceps) is found in southeastern Madagascar. This species is endangered due to the loss and fragmentation of its natural habitat and hunting. Eighteen nuclear microsatellite loci were isolated from genomic DNA derived from an animal from Mahabo Forest in Madagascar. Population genetic parameters were estimated from a population of white-collared lemur sampled at Vevembe Forest 7 years apart to evaluate the potential utility of this marker suite.

Differences in seasonal migration might promote reproductive isolation and differentiation by causing populations in migratory divides to arrive on the breeding grounds at different times and/or produce hybrids that take inferior migratory routes. We examined this question by quantifying divergence in song, colour, and morphology between sister pairs of North American migratory birds. We predicted that apparent rates of phenotypic differentiation would differ between pairs that do and do not form migratory divides. Consistent with this prediction, results from mixed effects models and Ornstein–Uhlenbeck models of evolution showed different rates of divergence between these groups; surprisingly, differentiation was greater among non-divide pairs. We interpret this finding as a result of variable rates of population blending and fusion between partially diverged forms. Ancient pairs of populations that subsequently fused are now observed as a single form, whereas those that did not fuse are observable as pairs and included in our study. We propose that fusion of two populations is more likely to occur when they have similar migratory routes and little other phenotypic differentiation that would cause reproductive isolation. By contrast, pairs with migratory divides are more likely to remain reproductively isolated, even when differing little in other phenotypic traits. These findings suggest that migratory differences may be one among several isolating barriers that prevent divergent populations from fusing and thereby increase the likelihood that they will continue differentiating as distinct species.

Migratory divides are contact zones between populations that use different routes to navigate around unsuitable areas on seasonal migration. Hybrids in divides have been predicted to employ intermediate and potentially inferior routes. We provide the first direct test of this hypothesis, using light-level geolocators to track birds breeding in a hybrid zone between Swainson's thrushes in western Canada. Compared to parental forms, hybrids exhibited increased variability in their migratory routes, with some using intermediate routes that crossed arid and mountainous regions, and some using the same routes as one parental group on fall migration and the other on spring migration. Hybrids also tended to use geographically intermediate wintering sites. Analysis of genetic variation across the hybrid zone suggests moderately strong selection against hybrids. These results indicate that seasonal migratory behaviour might be a source of selection against hybrids, supporting a possible role for migration in speciation.

Migratory divides are contact zones between breeding populations that use divergent migratory routes and have been described in a variety of species. These divides are of major importance to evolution, ecology and conservation but have been identified using limited band recovery data and/or indirect methods. Data from band recoveries and mitochondrial haplotypes suggested that inland and coastal Swainson's thrushes (Catharus ustulatus) form a migratory divide in western North America. We attached light-level geolocators to birds at the edges of this contact zone to provide, to our knowledge, the first direct test of a putative divide using data from individual birds over the entire annual cycle. Coastal thrushes migrated along the west coast to Mexico, Guatemala and Honduras. Some of these birds used multiple wintering sites. Inland thrushes migrated across the Rocky Mountains, through central North America to Columbia and Venezuela. These birds migrated longer distances than coastal birds and performed a loop migration, navigating over the Gulf of Mexico in autumn and around this barrier in spring. These findings support the suggestion that divergent migratory behaviour could contribute to reproductive isolation between migrants, advance our understanding of their non-breeding ecology, and are integral to development of detailed conservation strategies for this group.

Hybridization has recently been identified as a pervasive force in the evolution of primates. In this study, we characterized a hybrid zone between two species of brown lemur (Eulemur rufifrons and E. cinereiceps) in the Andringitra region of southeastern Madagascar using morphological traits. We immobilized animals along a north-south transect (∼80 km), scored them for their degree of hybridity using pelage traits and measured standard morphometric variables. Results from our study suggest that hybridization between E. rufifrons and E. cinereiceps is extensive, with the hybrid zone extending over 42.6 km and being composed mostly of later generation hybrids. We also identified significant variation between ancestral groups in our study: hybrid males exhibited longer tails than both parental species and sexual dimorphism in upper canine height favoring males was documented in E. rufifrons. These patterns could suggest that gene flow between parental and hybrid populations is relatively limited. Finally, significant differences between ancestral groups in relative body mass and skin-fold thickness were absent in our study, indicating that, as measured by these proxies, hybrids are equally as fit as parental forms. Based on these preliminary findings, the Andringitra hybrid zone could conform to the bounded superiority model of hybrid zone stability (i.e., it could be being maintained by selection favoring hybrids within transitional habitats). Accordingly, hybrids in Andringitra may be an unusual case among primates, representing a stable recombinant but distinct lineage. This conclusion has important implications for evolutionary processes within the brown lemur species complex. Am J Phys Anthropol, 2011. © 2011 Wiley-Liss, Inc.

Ecosystems services are threatened by the rapid degradation of tropical rainforests. In light of these threats, questions remain about how societies on the forest fringe who depend on provisioning services affect plant functional traits. This study assessed the relationship between plant functional traits, forest-dependent societies and provisioning ecosystem services along a forest–agriculture matrix gradient in tropical humid forests of Madagascar. Data were collected for six functional traits and six provisioning services. We evaluated functional diversity (FD) and utilitarian diversity (FD of provisioning services) along disturbance gradients. We also determined the traits most susceptible to loss along the gradient as well as the relationship between functional traits and provisioning services. The results showed that FD, utilitarian diversity and species richness decreased significantly across all modified habitats. There was a distinct suite of traits absent from intensely used habitats and those same traits were associated with the two most important provisioning services in the region (firewood and construction). The activities of people living on the forest fringe seem to be a strong selective force on trait loss in plant communities, which in turn will influence future species assembly and trait diversity and distribution. Moreover, this study suggests that it is possible to predict trait loss from plant communities in forests where degradation is mediated primarily through subsistence agriculture and resource extraction. Conservation efforts should recognize that forest degradation and deforestation are contextually specific, determined mostly by people’s efforts to maintain their basic livelihood, and therefore necessitate local-scale interventions that feed into landscape-scale policy initiatives.