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Abstract Divergent adaptation can promote ecological speciation if hybrids have reduced fitness because they are poorly adapted to either parental niche. We tested for ecologically dependent, postzygotic isolation between two subspecies of Swainson’s thrushes, which form a migratory divide and hybrid zone in western North America. To do this, we translocated backcrossed and admixed birds from the hybrid zone into the range of each subspecies in the beginning of fall migration. We estimated a proxy for their survival on migration and migratory behaviour using automated radio tracking. Apparent survival of birds in the two environments did not depend on their genomic ancestry, suggesting that Swainson’s thrushes’ divergent adaptation to different fall migration routes does not fit the classic model of ecological speciation. We propose an alternate scenario where ecological selection on migration may interact with intrinsic maladaptation in hybrids to cause hybrid survival on migration. By translocating birds from the same genomic backgrounds into different environments, our experiment also allowed us to distinguish between the effects of environmental relative to genetic contributors to their migratory behaviour. We found evidence that both genetic and environmental factors influence migratory behaviour, as an effect of genomic ancestry on initial migratory trajectories depended on the start location for migration but birds ultimately followed expected routes given their genomic ancestries. 

Abstract Seasonal migration is performed by taxonomically diverse groups across the planet’s oceans and continents. Migration has been hypothesized to promote speciation through a variety of mechanisms that may initiate reproductive isolation and population divergence, such as temporal or spatial migratory divides, migration “falloffs,” or the colonization of new, geographically isolated breeding areas.  Migration has also been implicated in recent population divergence within a handful of bird species; however, it is unknown whether migration is generally associated with higher speciation rates. We sought to test this question in two large clades of New World birds with diverse migratory phenotypes, the suboscines and the Emberizoidea, employing three state-of-the-art comparative methods of trait-based diversification: estimates of tip speciation rates using 1) BAMM and 2) ClaDS, and 3) hidden-state speciation extinction models. Our results differed across methods and across taxonomic scales, suggesting an acute need to corroborate inferences across different frameworks and data sets prior to concluding that a given trait has, in fact, promoted diversification. Overall, and based upon the majority of results across different methods, we conclude that there is no methodologically consistent evidence of faster speciation in migratory lineages in these groups.  We discuss the biological implications of this finding, as well as the challenges of inference posed by current trait-based diversification methods. 

Abstract Extrinsic postzygotic isolation, where hybrids experience reductions in fitness due to a mismatch with their environment, is central to speciation. Knowledge of genetic variants that underlie extrinsic isolation is crucial for understanding the early stages of speciation. Differences in seasonal migration are strong candidates for extrinsic isolation (e.g., if hybrids take intermediate and inferior routes compared to pure forms). Here, we used a hybrid zone between two subspecies of the songbird Swainson’s thrush (Catharus ustulatus) with different migratory routes and tests for viability selection (locus-specific changes in interspecific heterozygosity and ancestry mismatch across age classes) to gain insight into the genetic basis of extrinsic isolation. Using data from over 900 individuals we find strong evidence for viability selection on both interspecific heterozygosity and ancestry mismatch at loci linked to migration. Much of this selection was dependent on genome-wide ancestry; as expected, a subset of hybrids exhibited reduced viability, but remarkably, another subset appears to fill an unoccupied fitness peak within the species, exhibiting higher viability than even parental forms. Many of the variants that influence hybrid viability appear to occur in structural variants, including a putative pericentric inversion. Our study emphasizes the importance of epistatic interactions and structural variants in speciation. 

ABSTRACT Partial migration is a phenomenon where migratory and resident individuals of the same species co‐exist within a population, and has been linked to both intrinsic (e.g., genetic) as well as environmental factors. Here we investigated the genomic architecture of partial migration in the common blackbird, a songbird that comprises resident populations in the southern distribution range, partial migratory populations in central Europe, and exclusively migratory populations in northern and eastern Europe. We generated whole‐genome sequencing data for 60 individuals, each of which was phenotyped for migratory behavior using radio‐telemetry tracking. These individuals were sampled across the species' distribution range, including resident populations (Spain and France), obligate migrants (Russia), and a partial migratory population with equal numbers of migratory and resident individuals in Germany. We estimated genetic differentiation (F_ST) of single‐nucleotide variants (SNVs) in 2.5 kb windows between all possible population and migratory phenotype combinations, and focused our characterization on birds from the partial migratory population in Germany. Despite overall low differentiation within the partial migratory German population, we identified several outlier regions with elevated differentiation on four distinct chromosomes. The region with the highest relative and absolute differentiation was located on chromosome 9, overlappingPER2, which has previously been shown to be involved in the control of the circadian rhythm across vertebrates. While this region showed high levels of differentiation, no fixed variant could be identified, supporting the notion that a complex phenotype such as migratory behavior is likely controlled by a large number of genetic loci. 

ABSTRACT The application of high‐throughput sequencing to phylogenetic analyses is allowing authors to reconstruct the true evolutionary history of species. This work can illuminate specific mechanisms underlying divergence when combined with analyses of gene flow, recombination and selection. We conducted a phylogenomic analysis ofCatharus, a songbird genus with considerable potential for gene flow, variation in migratory behaviour and genomic resources. We documented discordance among trees constructed for mitochondrial, autosomal and sex (Z) chromosome partitions. Two trees were recovered on the Z. Both trees differed from the autosomes, one matched the mitochondria, and the other was unique to the Z. Gene flow with one species likely generated much of this discordance; substantial admixture betweenustulatusand the remaining species was documented and linked to at least two historic events. The tree unique to the Z likely reflects the true history ofCatharus; local genomic analyses recovered the same tree in autosomal regions with reduced admixture and recombination. Genes previously connected to migration were enriched in these regions suggesting transitions between migratory and non‐migratory states helped generate divergence. Migratory (vs. nonmigratory)Catharusformed a monophyletic clade in a subset of genomic regions. Gene flow was elevated in some of these regions suggesting adaptive introgression may have occurred, but the dominant pattern was of balancing selection maintaining ancestral polymorphisms important for olfaction and perhaps, by extension, adaptation to temperate climates. This work illuminates the evolutionary history of an important model in speciation and demonstrates how differential resistance to gene flow can affect local genomic patterns. 

Abstract Migratory divides, hybrid zones between populations that use different seasonal migration routes, are hypothesised to contribute to speciation. Specifically, relative to parental species, hybrids at divides are predicted to exhibit (1) intermediate migratory behaviour and (2) reduced fitness as a result. We provide the first direct test of the second prediction here with one of the largest existing avian tracking datasets, leveraging a divide between Swainson's thrushes where the first prediction is supported. Using detection rates as a proxy for survival, our results supported the migratory divide hypothesis with lower survival rates for hybrids than parental forms. This finding was juvenile‐specific (vs. adults), suggesting selection against hybrids is stronger earlier in life. Reduced hybrid survival was not explained by selection against intermediate phenotypes or negative interactions among phenotypes. Additional work connecting specific features of migration is needed, but these patterns provide strong support for migration as an ecological driver of speciation. 

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 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 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.