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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.
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The genetics of extrinsic postzygotic selection in a migratory divide between subspecies of the Swainson’s thrush
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.
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- PAR ID:
- 10657177
- Publisher / Repository:
- Nature Communications
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 16
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1038/s41467-025-63188-6
