Genetic recombination shapes complex hybrid effects across the pig genome

Genome and phenotype evolution during hybridization has been a central topic in evolutionary biology, yet the genetic mechanism underlying the hybrid effect variation remain elusive. Here we use the pig as a model and quantify hybrid effects by measuring the phenotypic difference between homozygotes and heterozygotes across 135 traits in 578 F2 individuals from a Eurasian pig cross population. We demonstrate that hybrid effect sizes follow an exponential distribution across the genome. The rate parameter (λ) of this exponential distribution exhibits a hump-shaped pattern with increasing levels of F0 genomic divergence, indicating a genomic transition from inbreeding depression to hybrid vigor and ultimately to hybrid depression. Further analysis reveals that genetic recombination is significantly correlated with the variation in λ, supporting a model in which both recombination and genomic divergence jointly shape the landscape of hybrid effects. Females display lower λ values, with a pronounced reduction in regions exhibiting hybrid depression, revealing a fundamental sex difference in Eurasian pig hybridization. We further show that the λ positively correlates with F2 heterozygote-to-homozygote genotype frequency ratio. This suggests that recombination may introduce advantageous hybrid effect in genetic backgrounds otherwise characterized by inbreeding depression or hybrid depression, resulting in asynchronous evolutionary paces across the genome.