Avian population genomics taking off: latest findings and future prospects

Birds are one of the most recognizable and diverse groups of organisms on earth. This group has played animportant role in many fields, including the development of methods in behavioral ecology and evolution-ary theory. The use of population genomics took off following the advent of high-throughput sequencingin 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. Wereview the latest findings in the population genomics of birds here, emphasizing questions related tobehavior, ecology, evolution, and conservation. Additionally, we include insights in trait mapping and theability to obtain accurate estimates of important summary statistics for conservation (e.g., genetic diversityand inbreeding). We highlight roadblocks that will need to be overcome in order to advance work on thepopulation genomics of birds and prospects for future work. Roadblocks include the assembly of morecontiguous reference genomes using long-reads and optical mapping. Prospects include the integration ofpopulation genomics with additional fields (e.g., landscape genetics, phylogeography, and genomicmapping) along with studies beyond genetic variants (e.g., epigenetics)

Migratory birds use head scans to detect the direction of the earth’s magnetic field

Night-migratory songbirds are known to use a magnetic compass [1–3], but how do they detect the reference direction provided by the geomagnetic field, and where is the sensory organ located? The most prominent characteristic of geomagnetic sensory input, whether based on visual patterns [4–7] or magnetite-mediated forces [8, 9], is the predicted symmetry around the north-south or east-west magnetic axis. Here, we show that caged migratory garden warblers perform head-scanning behavior well suited to detect this magnetic symmetry plane. In the natural geomagnetic field, birds move toward their migratory direction after head scanning. In a zero-magnetic field [10], where no symmetry plane exists, the birds almost triple their head-scanning frequency, and the movement direction after a head scan becomes random. Thus, the magnetic sensory organ is located in the bird's head, and head scans are used to locate the reference direction provided by the geomagnetic field

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology, and migratory behavior, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole-genome pooled sequencing of 262 individuals from 5 taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked if these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g., areas of low recombination). Consequently, studies employing genome scans to search for areas important for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation

Night-time neuronal activation of Cluster N in a day- and night-migrating songbird.

Magnetic compass orientation in a night-migratory songbird requires that Cluster N, a cluster of forebrain regions, is functional. Cluster N, which receives input from the eyes via the thalamofugal pathway, shows high neuronal activity in night-migrants performing magnetic compass-guided behaviour at night, whereas no activation is observed during the day, and covering up the birds' eyes strongly reduces neuronal activation. These findings suggest that Cluster N processes light-dependent magnetic compass information in night-migrating songbirds. The aim of this study was to test if Cluster N is active during daytime migration. We used behavioural molecular mapping based on ZENK activation to investigate if Cluster N is active in the meadow pipit (Anthus pratensis), a day- and night-migratory species. We found that Cluster N of meadow pipits shows high neuronal activity under dim-light at night, but not under full room-light conditions during the day. These data suggest that, in day- and night-migratory meadow pipits, the light-dependent magnetic compass, which requires an active Cluster N, may only be used during night-time, whereas another magnetosensory mechanism and/or other reference system(s), like the sun or polarized light, may be used as primary orientation cues during the day

The blackcap (Sylvia atricapilla) genome reveals a species-specific accumulation of LTR retrotransposons

Transposable elements are mobile genetic elements that have the ability to move around the genome, and as such can be a source of genome variability. Transposable elements (TEs) are ubiquitous and many are found within a wide variety of life. 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 this through a high-quality TE annotation of the Eurasian blackcap (Sylvia atricapilla), as our chromosome resolution reference genome allowed the reconstruction of difficult-to-assemble regions. We have the ability to distinguish species-specific and non-specific TEs. We investigate how these TE categories are distributed along the genome and evaluate their correlation with four genomic features: recombination rate, gene coverage, CpG island coverage and GC coverage. We found a marked difference between species-specific and non-specific TEs. While species-specific TEs were negatively correlated with both GC content and recombination rate, the correlation with recombination rate disappeared and turned positive for GC content when considering non-specific TEs

Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation

Migratory birds can use a magnetic compass for orientation during their migratory journeys covering thousands of kilometers. But how do they sense the reference direction provided by the Earth’s magnetic field? Behavioral evidence and theoretical considerations have suggested that radical-pair processes in differently oriented, light-sensitive molecules of the retina could enable migratory birds to perceive the magnetic field as visual patterns. The cryptochromes (CRYs) have been suggested as the most likely candidate class of molecules, but do CRYs exist in the retina of migratory birds? Here, we show that at least one CRY1 and one CRY2 exist in the retina of migratory garden warblers and that garden-warbler CRY1 (gwCRY1) is cytosolic. We also show that gwCRY1 is concentrated in specific cells, particularly in ganglion cells and in large displaced ganglion cells, which also showed high levels of neuronal activity at night, when our garden warblers performed magnetic orientation. In addition, there seem to be striking differences in CRY1 expression between migratory and nonmigratory songbirds at night. The difference in CRY1 expression between migrants and nonmigrants is particularly pronounced in the large displaced ganglion cells known to project exclusively to a brain area where magnetically sensitive neurons have been reported. Consequently, cytosolic gwCRY1 is well placed to possibly be the primary magnetic-sensory molecule required for light-mediated magnetoreception

A new model for magnetoreception

Certain migratory birds can sense the earth's magnetic field. The nature of this process is not yet properly understood. Here we offer a simple explanation according to which birds literally `see' the local magnetic field: Our model relates the well-established radical pair hypothesis to the phenomenon of Haidinger's brush, a capacity to see the polarisation of light. This new picture explains recent surprising experimental data indicating long lifetimes for the radical pair. Moreover there is a clear evolutionary path toward this field sensing mechanism: it is an enhancement of a weak effect that may be present in many species.Comment: 8 pages, 5 figures, version of final published pape

Human activity shapes the wintering ecology of a migratory bird

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 chal-lenges, the blackcap (Sylvia atricapilla) is a thriving migratory species. Its recent es-tablishment 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 investi-gated visitation behavior at garden feeding sites, inter-annual site fidelity, and move-ments within and across seasons. We analyzed migration tracks from 25 geolocators fitted to a subset of individuals to understand how garden behavior may impact sub-sequent 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 ex-clusively 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 mor-phological evolution. Supplemental feeding may have multifaceted benefits on win-ter 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

The evolutionary history and genomics of European blackcap migration

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

Population-specific association of Clock gene polymorphism with annual cycle timing in stonechats

Timing is essential for survival and reproduction of organisms across the tree of life. The core circadian clock gene Clk has been implicated in annual timing 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 set up to study associations of Clk with latitude, migration and annual-cycle timing within the stonechat species complex with trans-equatorial distribution range. Including 950 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 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