Inversion Polymorphisms Carried by Introduced Rainbow Trout Disrupt Hybrid Zones Between Native Species

Genomic mechanisms explaining why some hybrid zones remain stable while others collapse into hybrid swarms are poorly understood. In Montana's Kootenai River Basin, native interior redband trout (Oncorhynchus mykiss gairdneri; IRT) and westslope cutthroat trout (O. lewisi; WCT) are naturally sympatric and historically exhibited limited hybridization. However, the introduction of allopatric coastal rainbow trout (O. m. ssp.; CRT) has coincided with hybrid swarm formation. Using novel IRT linkage maps and 3489 individuals genotyped at 189,984 SNPs, we characterized the role of genome structure in hybridization among native and invasive taxa. Native IRT were fixed for the derived arrangement of a double inversion complex on chromosome 5 (Chr05), whereas introduced CRT and intraspecific hybrids retained the ancestral polymorphism associated with migratory behaviour. Widespread hybridization was primarily driven by intraspecific admixture among rainbow trout (RBT) taxa, rather than with other species, likely mediated by genomic structural variants introduced into IRT populations via CRT admixture. Specifically, Chr05 genotypes exhibited strong habitat stratification; migratory-associated haplotypes occurred primarily in migration-associated habitats, implicating dispersal as a key mechanism promoting introgression. We found evidence of selection against interspecific hybrids, possibly tied to interspecific inversions. Notably, WCT carried a distinct form of Chr05 that is colinear with the ancestral RBT form. Interspecific hybrids carrying both the WCT and ancestral RBT forms (WCT_A/RBT_A), despite being structurally homozygous, were rare (1.59%), suggesting selection or stronger genomic incompatibility. Ultimately, introduced intraspecific variation may facilitate introgression via dispersal while distinct interspecific structural arrangements maintain genomic barriers, restricting gene flow.