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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 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 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.