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Seasonal migration is a widespread behavior relevant for adaptation and speciation, yet knowledge of its genetic basis is limited. We leveraged advances in tracking and sequencing technologies to bridge this gap in a well-characterized hybrid zone between songbirds that differ in migratory behavior. Migration requires the coordinated action of many traits, including orientation, timing, and wing morphology. We used genetic mapping to show these traits are highly heritable and genetically correlated, explaining how migration has evolved so rapidly in the past and suggesting future responses to climate change may be possible. Many of these traits mapped to the same genomic regions and small structural variants indicating the same, or tightly linked, genes underlie them. Analyses integrating transcriptomic data indicate cholinergic receptors could control multiple traits. Furthermore, analyses integrating genomic differentiation further suggested genes underlying migratory traits help maintain reproductive isolation in this hybrid zone. 

Night-migrating songbirds utilize the Earth’s magnetic field to help navigate to and from their breeding sites each year. A region of the avian forebrain called Cluster N has been shown to be activated during night migratory behavior and it has been implicated in processing geomagnetic information. Previous studies with night-migratory European songbirds have shown that neuronal activity at Cluster N is higher at night than during the day. Comparable work in North American migrants has only been performed in one species of swallows, so extension of examination for Cluster N in other migratory birds is needed. In addition, it is unclear if Cluster N activation is lateralized and the full extent of its boundaries in the forebrain have yet to be described. We used sensory-driven gene expression based on ZENK and the Swainson’s thrush, a night-migratory North American songbird, to fill these knowledge gaps. We found elevated levels of gene expression in night- vs. day-active thrushes and no evidence for lateralization in this region. We further examined the anatomical extent of neural activation in the forebrain using 3D reconstruction topology. Our findings demonstrate that Swainson’s thrushes possess an extensive bilateral night-activated Cluster N region in the forebrain similar to other European avian species, suggesting that Cluster N is highly conserved in nocturnal migrants. 

Abstract Hybrid zones can be used to identify traits that maintain reproductive isolation and contribute to speciation. Cognitive traits may serve as post-mating reproductive isolating barriers, reducing the fitness of hybrids if, for example, misexpression occurs in hybrids and disrupts important neurological mechanisms. We tested this hypothesis in a hybrid zone between two subspecies of Swainson’s thrushes (Catharus ustulatus) using two cognitive tests—an associative learning spatial test and neophobia test. We included comparisons across the sexes and seasons (spring migration and winter), testing if hybrid females performed worse than males (as per Haldane’s rule) and if birds (regardless of ancestry or sex) performed better during migration, when they are building navigational maps and encountering new environments. We documented reduced cognitive abilities in hybrids, but this result was limited to males and winter. Hybrid females did not perform worse than males in either season. Although season was a significant predictor of performance, contrary to our prediction, all birds learned faster during the winter. The hypothesis that cognitive traits could serve as post-mating isolating barriers is relatively new; this is one of the first tests in a natural hybrid zone and non-food-caching species. We also provide one of the first comparisons of cognitive abilities between seasons. Future neurostructural and neurophysiological work should be used to examine mechanisms underlying our behavioral observations. 

Abstract The impact of climate change on spring phenology poses risks to migratory birds, as migration timing is controlled predominantly by endogenous mechanisms. Despite recent advances in our understanding of the underlying genetic basis of migration timing, the ways that migration timing phenotypes in wild individuals may map to specific genomic regions requires further investigation. We examined the genetic architecture of migration timing in a long-distance migratory songbird (purple martin,Progne subis subis) by integrating genomic data with an extensive dataset of direct migratory tracks. A moderate to large amount of variance in spring migration arrival timing was explained by genomics (proportion of phenotypic variation explained by genomics = 0.74; polygenic scoreR² = 0.24). On chromosome 1, a region that was differentiated between migration timing phenotypes contained genes that could facilitate nocturnal flights and act as epigenetic modifiers. Overall, these results advance our understanding of the genomic underpinnings of migration timing. 

Abstract Behavioral variation abounds in nature. This variation is important for adaptation and speciation, but its molecular basis remains elusive. Here, we use a hybrid zone between two subspecies of songbirds that differ in migration – an ecologically important and taxonomically widespread behavior---to gain insight into this topic. We measure gene expression in five brain regions. Differential expression between migratory states was dominated by circadian genes in all brain regions. The remaining patterns were largely brain-region specific. For example, expression differences between the subspecies that interact with migratory state likely help maintain reproductive isolation in this system and were documented in only three brain regions. Contrary to existing work on regulatory mechanisms underlying species-specific traits, two lines of evidence suggest that trans- (vs. cis) regulatory changes underlie these patterns – no evidence for allele-specific expression in hybrids and minimal associations between genomic differentiation and expression differences. Additional work with hybrids shows expression levels were often distinct (transgressive) from parental forms. Behavioral contrasts and functional enrichment analyses allowed us to connect these patterns to mitonuclear incompatibilities and compensatory responses to stress that could exacerbate selection on hybrids and contribute to speciation. 

Abstract Structural variants (SVs) are a major source of genetic variation; and descriptions in natural populations and connections with phenotypic traits are beginning to accumulate in the literature. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (a) characterized the genome-wide distribution, frequency, and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (b) used these SVs to study the genetics of seasonal migration. We detected >15 K SVs. Many SVs overlapped repetitive regions and exhibited evidence of purifying selection suggesting they have overall deleterious effects on fitness. We used estimates of genomic differentiation to identify SVs exhibiting evidence of selection in blackcaps with different migratory strategies. Insertions and deletions dominated the SVs we identified and were associated with genes that are either directly (e.g., regulatory motifs that maintain circadian rhythms) or indirectly (e.g., through immune response) related to migration. We also broke migration down into individual traits (direction, distance, and timing) using existing tracking data and tested if genetic variation at the SVs we identified could account for phenotypic variation at these traits. This was only the case for 1 trait—direction—and 1 specific SV (a deletion on chromosome 27) accounted for much of this variation. Our results highlight the evolutionary importance of SVs in natural populations and provide insight into the genetic basis of seasonal migration.