Adaptive coupling of chromosomal inversions with multilocus ecological, mating-bias, and hybrid-incompatibility genotypes facilitates sympatric speciation

Chromosomal inversions (CIs) are widespread structural variants that suppress recombination and maintain favorable allele combinations as tightly linked supergenes. They are increasingly recognized for their contributions to local adaptation and speciation, yet their role in sympatric speciation under ongoing gene flow remains unresolved. Here, we develop mathematical models and computer simulations to examine how polygenic architectures and CI invasion jointly shape the evolution of reproductive isolation (RI) in a two-niche model under disruptive ecological selection. Extending previous frameworks, we incorporate multilocus ecological traits, multilocus mating-bias traits, and multilocus hybrid-incompatibility genotypes, and evaluate the invasion fitness and evolutionary consequences of CIs capturing different combinations of locally adaptive alleles. We show that the evolutionary impact of CI invasion depends critically on how polygenic trait structure influences hybrid production and the strength of barrier mechanisms. Increasing the number of ecological or hybrid-incompatibility loci strengthens disruptive ecological selection and postzygotic incompatibility selection by generating more unfit hybrids, whereas increasing the number of mating-bias loci weakens premating selection because mating-bias hybrids remain viable within the same niche. Accordingly, CIs capturing ecological or hybrid-incompatibility alleles tend to reduce the effective number of loci, diminish hybrid loss, and weaken existing RI, whereas CIs capturing mating-bias alleles strengthen premating isolation by reducing the effective number of mating-bias loci. Importantly, CIs that couple alleles across distinct barrier mechanisms exhibit elevated invasion fitness and generate synergistic reinforcement and positive feedback among premating isolation, postmating isolation, and ecological divergence. These findings reconcile contrasting theoretical predictions by demonstrating that CIs can either facilitate or constrain sympatric speciation depending on how they reshape effective locus number and barrier coupling, and provide a unified framework for understanding how structural genomic variants interact with polygenic architectures to influence the origin and stability of reproductive isolation.