Adaptive evolution and loss of a putative magnetoreceptor in passerines.

Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, and Cry4a from a migratory songbird seems to show enhanced magnetic sensitivity in vitro compared to Cry4a from resident species. We investigate Cry and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modelling. Our analysis is based on 363 bird genomes and identifies different selection regimes in passerines. We show that Cry4a is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that are likely to have facilitated the evolution of an optimized sensory protein for night-time orientation in songbirds. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines), and thus identified a gene deletion, which might facilitate testing the function of Cry4a in birds. In contrast, the other avian Cry (Cry1 and Cry2) were highly conserved across all species, indicating basal, non-sensory functions. Our results support a specialization or functional differentiation of Cry4 in songbirds which could be magnetosensation.

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.

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.

Comparative analysis examining patterns of genomic differentiation across multiple episodes of population divergence in birds.

Heterogeneous patterns of genomic differentiation are commonly documented between closely related populations and there is considerable interest in identifying factors that contribute to their formation. These factors could include genomic features (e.g., areas of low recombination) that promote processes like linked selection (positive or purifying selection that affects linked neutral sites) at specific genomic regions. Examinations of repeatable patterns of differentiation across population pairs can provide insight into the role of these factors. Birds are well suited for this work, as genome structure is conserved across this group. Accordingly, we reestimated relative (FST ) and absolute (dXY ) differentiation between eight sister pairs of birds that span a broad taxonomic range using a common pipeline. Across pairs, there were modest but significant correlations in window-based estimates of differentiation (up to 3% of variation explained for FST and 26% for dXY ), supporting a role for processes at conserved genomic features in generating heterogeneous patterns of differentiation; processes specific to each episode of population divergence likely explain the remaining variation. The role genomic features play was reinforced by linear models identifying several genomic variables (e.g., gene densities) as significant predictors of FST and dXY repeatability. FST repeatability was higher among pairs that were further along the speciation continuum (i.e., more reproductively isolated) providing further insight into how genomic differentiation changes with population divergence; early stages of speciation may be dominated by positive selection that is different between pairs but becomes integrated with processes acting according to shared genomic features as speciation proceeds.

Candidate genes for migration do not distinguish migratory and non-migratory birds.

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.