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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.