Genome shock in a migratory songbird hybrid zone

Abstract

The genome shock hypothesis proposes that hybridization destabilizes genome regulation, leading to increased chromatin accessibility, derepression of transposable elements (TEs), and potential reductions in hybrid fitness, contributing to speciation. While extensively studied in plants, evidence in vertebrates is limited. Here, we tested this hypothesis in a hybrid zone between two subspecies of Swainson’s thrushes (Catharus ustulatus). We quantified genome-wide TE proportions, TE expression, and chromatin accessibility during both the migratory and non-migratory state using whole genome resequencing, RNA-seq, and ATAC-seq data from two migration-associated brain regions. Hybrids exhibited greater TE proportions, expression, and chromatin accessibility than parental lineages, providing the first direct evidence for genome shock in a wild avian system. TE expression and chromatin accessibility were positively correlated in all states and brain regions, but the strength of these patterns differed between states and tissues indicating that genome shock is context-dependent. Signatures of shock were localized in regulatory regions and associated with differential transcript factor binding sites linked to retinoic acid receptor signaling, a key pathway for seasonal and photoperiodic responses. Overlap between open chromatin, upregulated TEs and previously identified transgressively expressed genes in these hybrids suggest that genome shock extends beyond TE activation to directly affect gene expression. Our results motivate further investigation into genome shocks’ effects on genomic incompatibilities, hybrid fitness, and speciation.